Source-Sink Relationship in Intersubspecific Hybrid Rice
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1 250 Rice Science, 2006, 13(4): Source-Sink Relationship in Intersubspecific Hybrid Rice LI Ji-hang 1, 2, 3, XIANG Xun-chao 1, 2, 4, HE Li-bin 1, 2, LI Ping 1, 2 ( 1 Rice Research Institute, Sichuan Agricultural University, Wenjiang , China; 2 Key Laboratory of Southwest Crop Genetic Resource and Improvement, Ministry of Education, Sichuan Agricultural University, Ya an , China; 3 General Station of Agricultural Technology Extension in Sichuan, Chengdu , China; 4 Southwest University of Science and Technology, Mianyang , China) Abstract: Three indica restorer lines (Mianhui 725, Shuhui 527, Shuhui 881), an American rice variety Lemont and a javanica rice variety Xiangdali were crossed with japonica Kitaake, and five F 1 hybrids were obtained to study the photosynthetic and agronomic traits. The data on photosynthetic characteristics indicated that the net photosynthetic rate (Pn) of the five F 1 hybrids was significantly higher than that of their parents (or one of them) under high photosynthetic flux density (PFD); while the overall performance of hybrids was better than their respective parents in apparent quantum yield (AQY), carboxylation efficiency (CE) and CO 2 compensation point (CCP). Moreover, the photosynthetic performance of the five F 1 were different due to the variation in heredity and the typical indica-japonica hybrids, Mianhui 725/Kitaake and Shuhui 527/Kitaake, were better than the others on this aspect. The agronomic traits revealed that the five F 1 exhibited different heterosis, with Shuhui 881/Kitaake the largest sink followed by Mianhui 725/Kitaake, Shuhui 527/Kitaake, Lemont/Kitaake and Xiangdali/Kitaake. The production potential of indica-japonica hybrids was higher than that of the other two hybrids, which was consistent with the performance of Pn. However, the superior trait of indica-japonica hybrids on sink size has not been fully turned into high yield because of abnormal seed setting. Therefore, attention should be paid to the proper genome coordination and appropriate genetic distance so as to achieve super high yielding. Key words: rice; intersubspecific hybrid; source; sink; net photosynthetic rate; genetic distance; heterosis The yields of rice crop increased drastically after the beginning of rice green revolution symbolized by utilizing semi-dwarfing gene and the dissemination of hybrid rice. The increase in rice yield not only can handle the food crises in China but also across the globe. However, since the dissemination of hybrid rice in 1976, current dominant varieties have not yet overpass the earlier Nanyou 2 [1] in yield. The stagnant yield potential in southern indica rice-planting areas is due to the narrow genetic base of hybrid parents. For example, the three-line hybrid rice is still utilizing the heterosis of wild abortive cytoplasmic male sterile type and Southeast Asia restorer lines, or their hybrid generations [2-4]. In view of the population increase and limited land area in China, the increase in rice yield is utter most important. Therefore, the Super Rice Program was initiated to utilize the intersubspecific heteriosis Received: 14 April 2006; Accepted: 10 July 2006 Corresponding author: LI Ping (liping@cngk.com) in The grain filling rate of F 1 was not desirable mainly due to the lower transportation rate of photosynthetic products into production organs, and the exorbitant accumulation of dry-matter in culm and sheath. It turned into a major stymie to utilize intersubspecific heteriosis [5], indicating that intersubspecific rice failed to transfer productive superiority into economic superiority of yields. Moreover, the improvement in rice yields did not match well with the improvement of economic coefficient. For instance, comparing indica three-line hybrid rice with dwarfing indica rice, the increase in yields was mainly due to drastic improvement of large dry matters production and sink size with a slight decrease in economic coefficient [6]. Meanwhile, the large dry-matter production and large-sized sink means to demand a stronger capacity of dry-matter production. Therefore, Prof. Yuan pointed out that the increase in source is vital to improve yield [2]. In this study, we crossed japonica rice to maternal parents with genetic differences, and F 1 hybrids were obtained to analyze the source and sink relationship in intersubspefic
2 LI Ji-hang, et al. Source-Sink Relationship in Intersubspecific Hybrid Rice 251 hybrid rice. Moreover, the photosynthetic characteristics and agronomic performance in intersubpecific hybrid rice were also discussed in order to provide theoretic base for utilizing intersubspecific heterosis. MATERIALS AND METHODS Materials and experiment designs The paternal parent japonica rice Kitaake and the maternal parents including three indica restorer lines, (Mianhui 725, Shuhui 527, and Shuhui 881), one special American japonica rice Lemont, and one javanica rice Xiangdali belonging to tropic japonica were used in this experiment. The basic parent of Shuhui 527 and Mianhui 725 was indica rice without japonica rice consanguinity, while the basic parent of Shuhui 881 was indica rice with japonica rice consanguinity. All the parental materials were crossed in 2002 in Hainan Province and five F 1 hybrids were obtained. The further experiment was conducted in 2003 at Rice Research Institute of Sichuan Agricultural University. The five F 1 and maternal materials were sown in the mid of April and transplanted in the mid of May; while Kitaake was sown in the mid of June and transplanted in first ten days of July. All materials were planted in the same field with 3 replications with complete randomize block design. The seedlings were transplanted at 33 cm wide row spacing and 10 cm narrow rows spacing with 16 cm plant spacing and one plant per hill. The crop management was pursuant to conventional field mode. Observation method of photosynthesis curve The determination was performed at 9:00-11:30 a.m. with Li-6400 portable photosynthesis determination system at the initial-heading stage. Artificial lighting source was adopted at 32. To obtain the response curve of Pn to PFD, the photosynthetic rates were determined under a series of light intensity (PFD) [50, 150, 200, 400, 600, 800, 1000, 1200, 1500 µmol/(m 2 s)] in leaf chamber, and the concentration of CO 2 at 400 µmol/mol. AQY of each sample was obtained under low PFD [ µmol/(m 2 s)]. Then, CO 2 concentrations were changed to 400, 300, 200, 150, 100, 50 µmol/mol, and the PFD to 1200 µmol/(m 2 s). The CE and CCP were valued through the response curve of Pn at low CO 2 concentration ( µmol/mol). The above whole processes were automatically performed in the closedpath air system. Observation of agronomic traits and determination of soluble carbohydrates Five plants were randomly selected from every plot at the initial-heading stage and maturity stage. The plants were divided into four parts (green leaves, yellow leaves, culms and sheathes, and panicles) after cutting root. The samples were dried at 105 for 30 min, then at 80 for 48 h and weighed at last. The plant heights, number of effective panicles, number of grains per panicle, seed setting rate and 1000-grain weight of each F 1 hybrid were determined at the maturity stage. Heterosis of agronomic traits was computed according to the following formula: heterobeltiosis = (mean value of F 1 -mean value of the better parent) / mean value of the better parent 100%. Soluble carbohydrate content of each internode base of the main panicle was detected using the anthrone-colorimetric method at the maturity stage, which was repeated in thrice and the mean value was calculated. RESULTS Photosynthetic characteristics of F 1 and their parents The Pn of the parents and five F 1 increased with the increase in PFD with greatly under the low PFD (Fig. 1). Under the low PFD the four F 1 exhibited significant difference to their parents (or one of the parents) in AQY except for Shuhui 881/Kitaake (Table 1), while Xiangdali/ Kitaake had a lower AQY than the male parent Kitaake. On the other hand, at high level of PFD the increase in parental Pn was slow and stable relatively. On the whole, the Pn of the five F 1 individuals was higher than their parents (though Xiangdali/Litaake and Lemont/Kitaake were higher than that of their maternal parents only), while under high PFD conditions, the Pn increased gradually, indicating that F 1 were superior in Pn to their parents.
3 252 Rice Science, Vol. 13, No. 4, 2006 Fig. 1. Response of net photosynthetic rate to photo flux density in the parents and the five F 1 hybrids. The photosynthesis curves differed among different F 1 hybrids. Under the conditions of low PFD the curves of all F 1 climbed rapidly with the increase of photons flux according to AQY from Table 1. Shuhui 527/Kitaake ranked the first, followed by Mianhui 725/Kitaake, Lemont/Kitaake, Shuhui 881/ Kitaake, and Xiangdali/Kitaake. Moreover, for light saturation photosynthetic rate of the five F 1, the order was as follows: Shuhui 527/Kitaake > Mianhui 725/Kitaake>Shuhui 881/Kitaake>Lemont/Kitaake > Xiangdali /Kitaake. These results indicated the largest photosynthetic capacity in indica-japonica hybrid F 1 than the other F 1 (Table 1). The data revealed that the CE of all F 1 was significantly higher than that of their maternal parents (Table 1). The CE of three F 1 (Mianhui 725/Kitaake, Shuhui 527/Kitaake, and Shuhui 881/Kitaake) was higher than that of the paternal parent Kitaake. CCP of the five F 1 was lower than that of the maternal parents. However, the CCP of Mianhui 725/Kitaake and Xiangdali/Kitaake were higher than that of male parent Kitaake, while the CCP of the rest three F 1 showed no obvious difference compared with paternal parent. The results of photosynthetic indexes indicated an apparent heterosis in F 1, and most of them performed better than their parents. In comparison among the five F 1, the intersubspecific hybrid crosses between indica and japonica rice (Mianhui 725/Kitaake, Shuhui 527/Kitaake, Shuhui 881/Kitaake) showed obvious heterosis over the other two hybrid crosses, Xiangdali/Kitaake and Lemont/ Table 1. Apparent quantum yield, carboxylation efficiency (CE), CO 2 compensation point and saturation photosynthetic rate of the five F 1 hybrids and their parents. Material Apparent quantum yield Carboxylation efficiency CO 2 compensation point Saturation photosynthetic rate (mol/m 2 s) (µl/l) (µmol CO 2/m 2 s) Mianhui Mianhui 725/Kitaake **(*) **(**) 54.58**(*) 20.82**(**) Shuhui Shuhui 881/Kitaake **(**) 59.43** 18.79**(**) Shuhui Shuhui 527/Kitaake **(**) **(**) 58.20** 20.90**(**) Lemont Lemont/Kitaake ** * 57.29** 15.09**(*) Xiangdali Xiangdali/Kitaake *(**) ** 64.99**(*) 12.20**(**) Kitaake * and ** represent significance at P<0.05 and P<0.01 levels respectively ; * or ** indicates the significance with female parent(s), (*) or (**) with Kitaake.
4 LI Ji-hang, et al. Source-Sink Relationship in Intersubspecific Hybrid Rice 253 Kitaake (cross among different ecotype japonica rice), while Shuhui 881 had japonica consanguinity and Shuhui 881/Kitaake was slightly inferior to typical indica-japonica intersubspecific hybrid crosses, Mianhui 725/Kitaake and Shuhui 527/ Kitaake. The present results confirmed the notion that the larger genetic difference among parents, the stronger heterosis in F 1, which refers to a relatively strong photosynthetic assimilation capacity. Performances of agronomic traits and sink As shown in Table 2, the greatest plant height was noted in Shuhui 881/Kitaake followed by Mianhui 725/Kitaake, which showed no disparity compared with Shuhui 527/Kitaake. Lemont/Kitaake recorded the lowest value equivalent to Xiangdali/ Kitaake. However, Lemont/Kitaake exhibited the maximum heterobeltiosis, amounting to 34.7%, while Xiangdali/Kitakke exhibited negative heterosis. The heterosis of indica-japonica cross was superior to others in terms of plant height. Although the five F 1 had a better performance in panicle length than male parent, but the heterobeltiosis was not so obvious. Other than Mianhui 725/Kitaake showed 13.0% heterobeltiosis, the rest hybrids exhibited no or negative heterobeltiosis. Moreover, the panicle length of the five F 1 was not significantly different (Table 3). The present data showed that the hybrid performance was differed in number of effective panicles and grains per panicle, which are the two crucial agronomic traits associated with final yields. The number of effective panicles was higher in Shuhui 881/Kitaake and Mianhui 725/Kitaake, followed by Shuhui 527/Kitaake, which showed no significant difference with Lemont/Kitaake and Xiangdali/Kitaake. Shuhui 881/Kitaake performed 14.5% positive heterosis, while the rest four F 1 exhibited no difference or negative heterosis over their parents. The number of grains per panicle was the greatest in Shuhui 881/Kitaake among the five F 1 and the lowest in Xiangdali/Kitaake. Among all the F 1 only Shuhui 527/ Kitaake showed 22.3% heterobeltiosis. Among the five F 1, the greatest 1000-grain weight was noted in Xiangdali/Kitaake and the lowest in Lemont/ Kitaake. There was no heterosis or just negative heterosis over parents. In this paper, we viewed the product of the number of effective panicles, number of grains per panicles and 1000-grain weight as sink size, which served as theoretical yield index of candidate parent and F 1. The results indicated that F 1 exhibited the greatest heterobeltiosis over parents in sink size. Mianhui 725/Kitaake exhibited the strongest heterobeltiosis in terms of sink size followed by Xiangdali/Kitaake, Shuhui 881/Kitaake, Lemont/ Kitaake and Shuhui 527/Kitaake. However, the sink size was different in the five F 1. The overall performance of sink size was the highest in Shuhui 881/Kitaake followed by Mianhui 725/Kitaake, Table 2. Performances on agronomic traits of the 5 F 1 hybrids and their parents. Material Panicle Plant height No. of effective No. of grains grain Sink size Seed setting length (cm) panicles per m 2 per panicle weight (g) (kg/m 2 ) rate (%) (cm) Mianhui Mianhui 725/Kitaake 136.2(**) 26.09*(**) 498.5** 178.6(**) 29.40(*) 2.617**(**) 14.5**(**) Shuhui Shuhui 881/Kitaake 150.2**(**) 25.14(**) 516.7**(*) 192.4(**) 28.88**(*) 2.865**(**) 63.1(**) Shuhui Shuhui 527/Kitaake 136.7**(**) 23.40*(**) 323.7** 172.2**(**) 30.38*(**) 1.694(**) 24.9**(**) Lemont Lemont/Kitaake 128.3**(**) 23.79(**) 320.7(**) 181.3(**) 25.37* 1.475*(**) 41.2**(**) Xiangdali Xiangdali/Kitaake 126.7**(**) 24.75**(**) 337.4**(**) 97.96(**) 44.66**(**) 1.476**(**) 82.7** Kitaake *, ** represent significance at P<0.05 and P<0.01 levels respectively; * or ** indicate the significance with female parent(s), (* ) or (**) with Kitaake; Sink size = No. of effective panicles No. of grains per panicle Seed setting rate 10-6.
5 254 Rice Science, Vol. 13, No. 4, 2006 Table 3. Analysis on heterobeltiosis in agronomic traits of the five F 1 hybrids. Trait Heterobeltiosis (%) Mianhui 725/Kitaake Shuhui 881/Kitaake Shuhui 527/Kitaake Lemont/Kitaake Xiangdali/Kitaake Plant height Panicle length No. of effective panicles No. of grains per panicle grain weight Sink size Seed setting rate Table 4. Multiple comparisons on agronomic traits of the five F 1 hybrids. Materials Plant height Panicle No. of effective No. of grains 1000-grain Sink size Seed setting rate (cm) length (cm) panicle per m 2 per panicle weight (g) (kg/m 2 ) (%) Mianhui 725/Kitaake B a A B B B 14.5 E Shuhui 881/Kitaake A ab A A B A 63.1 B Shuhui 527/Kitaake B b B B B C 24.9 D Lemont/Kitaake C ab B AB C D 41.2 C Xiangdali/Kitaake C ab B C A D 82.7 A Values followed by the same uppercase and lowercase letters mean no significant difference at P<0.01 and P<0.05 levels respectively. Shuhui 527/Kitaake, and Xiangdali/ Kitaake, which was equal to Lemont/Kitaake. Therefore the indica-japonica crosses ranked the first due to the contribution of number of effective panicles. Though the sink size of Shuhui 527/Kitaake was almost similar to Lemont/Kitaake and Xiangdali/Kitaake, but their difference was highly significant. This was mainly due to Shuhui 527/Kitaake, which was superior in 1000-grain weight to Lemont/Kitaake, and superior to Xiangdali/Kitaake in number of grains per panicle. Though Xiangdali/Kitaake performed outstandingly in 1000-grain weight, but the poor number of grains per panicle constrained the heterosis. Moreover, Mianhui 725 / Kitaake and Shuhui 881/ Kitaake differed in sink size mainly attributed to difference in the number of grains per panicle compared with the three indica-japonica crosses, while the difference of sink size between Mianhui 725 / Kitaake and Shuhui 527 / Kitaake was to number of effective panicles. The sink size was nothing but a theoretic yield, and the real yield of indica-japonica crosses was constrained due to the poor seed setting rate. The indica-japonica hybrid Shuhui 881/Kitaake, next to Xiangdali/Kitaake, performed better seed setting rate than other two indica-japonica F 1 generations because of its consanguinity relationship with japonica rice. Character of dry matter transportation The Mianhui 725/Kitaake recorded the lowest seed setting rate with the greatest soluble carbohydrates and an obvious content increase in culm weight (Table 5). In contrast, the seed-setting rate was the maximum in Xiangdali/Kitaake, while the soluble carbohydrates content was lowest with the minimum increase in culm weight. The culm weight of each hybrid increased at the late stage of plant growth. The higher seed setting rate, the smaller increase of dry matter in culm and the lower content of soluble carbohydrates. Though Shuhui 881/Kitaake, Mianhui 725/Kitaake and Shuhui 527/Kitaake were indica-japonica intersubspecific hybrids, dry matter transportation of Shuhui 881/Kitaake was effective than that of the other two hybrids. The results of soluble carbohydrates content determination confirmed that the massive dry matter accumulation in culms of intersubspecific hybrids is due to constrained transportation of assimilates.
6 LI Ji-hang, et al. Source-Sink Relationship in Intersubspecific Hybrid Rice 255 Table 5. Seed setting rate and dry matter accumulation in culms of the five F 1 hybrids. Material Seed setting rate (%) Dry matter accumulation in culm (g) Soluble carbohydrate in culm (mg/l) Mianhui 725/Kitaake Shuhui 881/Kitaake Shuhui 527/Kitaake Lemont/Kitaake Xiangdali/Kitaake DISCUSSION Though light is necessary for plant growth, high light can disturb the photosynthetic system [8]. The light with high intensity may lead to decrease in the photosynthesis and increase in photooxidation, which significantly affects the rice yield [9]. We have noted that the Pn of F 1 hybrid was not only higher than that of parents but also showed an increasing trend under high PFD conditions (Fig. 1), indicating that the solar energy conversion rate of F 1 hybrids is higher over parents under high light intensity. Moreover, the further observation of CE and CCP showed that maternal parent was significantly different with the F 1. CE is constrained by Rubisco activity and activation degree. The change in CE can be helpful to predict the amount and activity of Rubisco [10-11], i.e. higher CE means higher Rubisco activity or higher quantity of Rubisco in leaves, and higher assimilation of CO 2. [12-13] Previous studies indicated a significant relationship between Rubisco activity and change in net photosynthetic rate. It can be suggested that F 1 can reach a relatively high Pn due to the good capacity of carbon dioxide assimilation in mesophyll cell. In this study, a japonica male parent has been crossed with several different ecotype maternal parents to get F 1 possessing genetic differences. Heterosis of F 1 in terms of agronomic traits and photosynthetic characteristics represents the genetic difference between parents. Indica-japonica intersubspicific F 1 (Mianhui 725/Kitaake, Shuhui 881/Kitaake, and Shuhui 527/Kitaake) exhibited strong competitive hererosis over the other two F 1 (Lemont/Kitaake and Xiangdali/Kitaake) in plant height, number of effective panicles, sink size and so on. However, greater genetic distance had also affected the seed-setting rate in the F 1 of indicajaponica. Meanwhile, the poor seed-setting rate restrained the transformation of biological source to economical yield in indica-japonica F 1 and hampered the utilization of heterosis among inter-subspecies. The detection of soluble carbohydrates content confirmed the massive dry matters accumulation in culms of intersubspecific hybrids. Compared with the other two indica-japonica hybrids, Shuhui 881/ Kitaake had heterosis not only in sink size and in seed setting rate, amounting to 63.1% next to Xiangdali/Kitaake, but also in transportation of assimilates. This confirmed the utilization of heterosis in intersubspecies crossing as an effective channel, more rather parents should have an appropriate genetic distance when utilizing heterosis in intersubspecific hybrid as a whole. The Breeding Theory of Intersubspecies Large- Panicle Hybrid Rice was proposed by Prof. Zhou [14], which is an important method for selecting and breeding super rice domestically. Later he proposed that the breeders should select large-panicle intersubspecific crosses; proportion of japonica rice consanguinity not exceed 1/4 under parental genetic background, and not more than 1/8 among hybrids. As a result, the selection of parents with distant pedigree relation can provide a base for super heterosis if we want to get the future super rice. In addition, coordinating parental genetic composition is also crucial to fulfill desirable harmony between hybrid genomes. ACKNOWLEDGEMENTS This work was supported by National High-Tech Research and Development Program (863) of China (Grant Nos. 2003AA212030, 2004AA207110) and
7 256 Rice Science, Vol. 13, No. 4, 2006 Program for Changjiang Scholars and Innovative Research Team in University (Grant No. IRT0453). REFERENCES 1 Xiao G Y, Yuan L P, Deng X X, Luo R L. Studies on the heterosis of indica /javanica and japonica/javanica hybrid rice: Ⅱ. Analysis of the heterosis of agronomic traits. Acta Agron Sin, 2003, 29(2): (in Chinese with English abstract) 2 Yuan L P. Hybrid Rice. Beijing: China Agricultural Press, (in Chinese) 3 Sun C Q, Jiang T B, Chen L, Wu C M, Li Z C, Wang X K. Studies on the relationship between heterosis and genetic differentiation in hybrid rice (Oryza sativa L.). Acta Agron Sin, 2000, 6(6): (in Chinese with English abstract) 4 Zeng Q C, Zhou K D, Zhu Z, Luo Q. Current status in the use of hybrid rice heterosis in China. Chinese J Rice Sci, 2000, 14 (4): (in Chinese with English abstract) 5 Yuan L P. Development in two-line hybrid rice research in China. Sci Agric Sin, 1990, 23(3): 1-6. (in Chinese with English abstract) 6 Zhu Q S, Zhang Z J, Yang J C, Cao X Z, Lang Y Z, Wang Z C. Source-sink characteristics to the yield in inter-subspecific hybrid rice. Sci Agric Sin, 1997, 30(3): (in Chinese with English abstract) 7 Li H S, Sun Q, Zhao S J. Principles and Techniques of Plant Physiological and Bio-chemical Experiment. Beijing: Higher Education Press, 1999: (in Chinese) 8 Ogren E, Evans J R. Photoinhibition in situ in six species of Eucalyptus. Aust J Plant Physiol, 1992, 19: Ji B H, Jiao D M. Varietal differences in photochemical efficiency of PS Ⅱ and features of CO 2 exchange in rice leaves under photoinhibitory conditions. Chinese J Rice Sci, 1998, 12(2): (in Chinese with English abstract) 10 Wang Z. Plant Physiology. Beijing: China Agricultural Press, 2000: (in Chinese) 11 von Caemmerer S, Farquhar G D. Some relationship between the biochemistry of photosynthesis and the gas exchange of leaves. Planta, 1981, 153: Weng X Y, Jiang D A. Regulation of Rubisco activity and diurnal changes of photosynthetic rate in rice by ecology factors. J Zhejiang Agric Univ: Agric & Life Sci, 2002, 28(4): (in Chinese with English abstract) 13 Weng X Y, Jiang D A, Lu Q. Influence of enzymes and relative factors on diurnal variation of photosynthetic rate in rice. J Biomath, 1999, 14(4): (in Chinese with English abstract) 14 Zhou K D, Wang X D. Research on subspecific heavy ear hybrid rice. Chengdu: Sichuan Science and Technique Publisher, 1997: (in Chinese)
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