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Evaluation of Genetic Variation Among Wild Populations and Local Varieties of Rice

Evaluation of Genetic Variation Among Wild Populations and Local Varieties of Rice Rice (2011) 4:170–177 DOI 10.1007/s12284-011-9067-x Evaluation of Genetic Variation Among Wild Populations and Local Varieties of Rice Takashige Ishii & Takashi Hiraoka & Tomoyuki Kanzaki & Masahiro Akimoto & Rieko Shishido & Ryo Ishikawa Received: 21 October 2011 /Accepted: 1 November 2011 /Published online: 19 November 2011 Springer Science+Business Media, LLC 2011 Abstract Cultivated rice (Oryza sativa L.) is derived from Introduction Asian wild rice (Oryza rufipogon Griff). Vietnamese local varieties and wild natural populations in Vietnam and Most crop species were originally derived from wild Myanmar were examined to evaluate the levels of genetic species. In the early days of domestication, primitive variation in cultivated and wild rice. In total, 222 Vietnamese farmers may have unconsciously chosen desirable plants local varieties were analyzed with ten microsatellite markers. based on several simple traits related to shattering habit, Using marker genotype and gene diversity data, the local seed dormancy, and seed size. However, the domestication varieties were differentiated based on geographical distribu- and selection process led to a rapid reduction in the genetic tion, cropping season, and human preference. A total of 976 diversity of crop species (Tanksley and McCouch 1997). wild plants were collected at six natural sites of wild Wild species maintain many genes that have been lost populations (three each in Myanmar and Vietnam), and the during domestication. Among them, trait-improving quan- degrees of variation among populations were analyzed with titative trait loci from wild relatives have been identified in five microsatellite markers. Phylogenetic analyses revealed various crops (Xiao et al. 1996, 1998; Tanksley et al. 1996). wide genetic differentiation among wild populations. The Such studies suggest that wild species still maintain many diversity values detected in a single wild population in beneficial alleles for future plant breeding. Vietnam were higher than those in whole Vietnamese local Oryza rufipogon is the ancestral wild species of varieties. These results indicate that wild rice has much cultivated rice, Oryza sativa (Oka 1988). They share the greater genetic variation than cultivated rice. same AA genome and show high levels of cross compat- ibility. Therefore, O. rufipogon may be the most important . . . Keywords Genetic variation Rice Local variety Wild wild genetic resource for rice breeding programs, because rice (Oryza rufipogon) its useful genes can be easily transferred by crossing. Although cultivated rice has less genetic variation than wild rice, local varieties have maintained many useful traits. : : : T. Ishii (*) T. Hiraoka T. Kanzaki R. Ishikawa Local varieties are cultivated forms developed by adapta- Graduate School of Agricultural Science, Kobe University, tion to the natural and cultural environment in each area Rokkodai, Nada-ku, and are more genetically diverse than modern breeding Kobe 657-8501, Japan e-mail: tishii@kobe-u.ac.jp varieties. Molecular markers have become powerful tools for M. Akimoto investigating genetic diversity among crop species. In Obihiro University of Agriculture and Veterinary Medicine, particular, microsatellite or simple sequence repeat (SSR) Inada, Obihiro 080-8555, Japan markers are useful for revealing intra- and inter-specific variation because they are codominant with high levels of R. Shishido allelic diversity (McCouch et al. 1997). Microsatellites are College of Bioresource Science, Nihon University, tandemly arranged repeats of short DNA motifs (1–4bpin Kameino, length) that frequently exhibit variation in the number of Fujisawa 252-8510, Japan Rice (2011) 4:170–177 171 repeats at a locus (Temnykh et al. 2001). Therefore, we and South Vietnam. According to the report, North Vietnam used microsatellite markers to evaluate genetic variation in local varieties were classified into two groups, “Fifth month rice. rice” and “Tenth month rice”. The former was grown First, we analyzed 222 local varieties originated from during the dry season, whereas the latter during rainy various areas in Vietnam. They were collected more than season. South Vietnam local varieties were divided into 50 years ago by the late Prof. Hamada, Hyogo University several groups based on the growing period during the of Agriculture, Japan, during a scientific expedition to rainy season and seed characters (“Early rice”, “Half season Indo-China. They are suitable materials for analyzing rice”, “Season rice”, “Late rice”, and “Glutinous rice”). genetic variation among local varieties before introducing Hamada (1965) classified “Glutinous rice” as South modern breeding methodologies. As for wild species of O. Vietnam varieties; however, half of them came from North rufipogon, many studies have been conducted to reveal the Vietnam according to the collection sites. Therefore, in this genetic differentiation among Asian accessions (Ishii et al. study, “Glutinous rice” was further divided into two groups, 2001; Sun et al. 2002; Cai et al. 2004). They usually used “Glutinous rice N” and “Glutinous rice S” for North and seed/plant materials derived from wild rice accessions South Vietnam, respectively. maintained in germplasm institutes or seed banks, but these accessions do not represent the features of natural wild rice. DNA extraction Wild natural populations in southern China were investi- gated by several research groups (Song et al. 2003; Zhou et Total DNA of the local variety was extracted from seed al. 2003;Gao 2004); however, those in the major specimen. For each variety, the embryo segment was distribution area of O. rufipogon have never been analyzed removed from a single seed and ground in 100 μlof in detail. In this study, a large-scale survey on wild rice was extracting solution containing 20 mM Tris–HCl (pH 8.0), carried out using 976 individuals from six natural popula- 5 mM EDTA, 400 mM NaCl, 0.3% SDS, and 200 μg/ml tions in Myanmar and Vietnam, and genetic variation proteinase K. The supernatant was used directly as the among wild rice populations was evaluated. In addition, template for PCR. the degree of genetic variation in wild rice was compared with that in local varieties. Research sites for the wild rice populations Research trips to collect wild rice were made to Myanmar Materials and methods in 2008 and Vietnam in 2007. Based on various population factors, such as ecotype (annual or perennial), size and Local varieties degree of disturbance, three research sites each in Myanmar (PT-1, YG-23, and AK-18) and Vietnam (CT-61, CT-65, In total, 222 Vietnamese local rice varieties were used and CT-67) were established for wild rice observations (Table 1). They were collected by the late Prof. Hamada, (Fig. 1). Environmental and geographical information for Hyogo University of Agriculture, in 1957 and 1958. Their these six observation sites is shown in Table 2. origins and ecological characteristics were described in a research report titled “Rice in Mekong Valleys” by Hamada Wild rice sample collection (1965). At the time of collection, Vietnam comprised North At each site, leaves were collected from the different plants Table 1 Vietnamese local varieties used in this study at 1–4-m intervals according to population size. In total, 976 wild natural plants from the six sites in Myanmar and Region Group Number of varieties Vietnam were surveyed. The number of samples ranged from 80 (CT-65) to 280 (YG-23), with an average of 162.6 North Fifth month rice 35 (Table 2). The collected leaf samples were crushed with a Tenth month rice 37 wooden hammer, and the leaf extract was fixed on an FTA Glutinous rice N 14 card (GE Healthcare). Samples were brought back to the South Early rice 33 laboratory, and small discs that were punched out from the Half season rice 27 FTA cards were used directly as PCR templates. Season rice 53 Late rice 12 Polymorphism detection using SSR markers Glutinous rice S 11 Total 222 Ten SSR markers (RM2, RM29, RM31, RM60, RM201, Classified by Hamada (1965) RM208, RM225, RM232, RM237, and RM241) were used. 172 Rice (2011) 4:170–177 Fig. 1 Geographical location of the wild rice populations studied in Myanmar and Vietnam. Of these, RM29 and RM208 are located on chromosome 2, 0.5 U of NovaTaq (Shimadzu, Japan). Amplification was and RM60 and RM232 on chromosomes 3. However, they performed with an MP Thermal Cycler (TaKaRa Bio, are not linked because their map distances are much more Japan) as follows: 94°C for 5 min, followed by 35 cycles of than 50 cM (Chen et al. 1997). Five SSR markers (RM31, 94°C for 1 min, 55°C for 1 min, 72°C for 2 min, and RM60, RM201, RM208, and RM237) were used for the ending with 5 min at 72°C for the final extension. The wild rice survey. PCR was performed in a 10–15 μl mixture amplified products were electrophoresed on 4% polyacryl- containing 1 μM of each primer, a half volume of 2× amide gels, and the banding pattern was visualized using a Ampdirect plus buffer (Shimadzu, Japan), 1 μl of template non-radioactive silver staining method, as described by DNA (or a small disc punched out from the FTA card), and Panaud et al. (1996). Table 2 Site information on wild rice populations in Myanmar and Vietnam Site Ecotype Population size Habitat Number of samples Latitude Longitude Myanmar PT-1 Perennial >3 km Deep water 180 17°03′52.5″ 95°35′20.3″ YG-23 Perennial c.a. 200 m Road-side swamp 280 17°08′49.1″ 96°17′28.4″ AK-18 Annual c.a. 150 m Paddy side 156 20°15′02.7″ 92°49′13.9″ Vietnam CT-61 Perennial c.a. 250 m Orange farm ditch 140 10°20′45.8″ 105°56′06.7″ CT-65 Perennial c.a. 3 km Canal (discontinuous) 80 09°46′48.9″ 105°38′02.9″ CT-67 Perennial c.a. 1.5 km Deep water 140 10°42′43.8″ 105°30′16.1″ Rice (2011) 4:170–177 173 Table 3 Average dissimilarity values within Vietnamese local variety groups Group North Vietnam South Vietnam Overall Fifth Tenth Glu N Early Half Season Late Glu S means Average dissimilarity 0.32 0.49 0.44 0.45 0.41 0.42 0.41 0.47 0.51 Fifth Fifth month rice, Tenth Tenth month rice, Early Early rice, Half Half season rice, Season Season rice, Late Late rice, Glu N Glutinous N, Glu S Glutinous S Evaluation of genetic variation within local variety groups Cultivated rice is a self-pollinating crop, whereas wild and wild populations ancestral O. rufipogon is cross-pollinating. Therefore, genetic variation within groups (or populations) was also Genetic variation within local variety groups was studied examined based on gene diversity, which can be applied to based on the dissimilarity of SSR electromorph allele sizes. plants with any pollinating system (Nei 1987). The gene The ratio of common fragments was calculated as a diversity values were calculated as follows: similarity index according to the following formula: H ¼ 1  x i ij F ¼ 2B =A j¼1 ij ij ij where A and B are the number of total and common where x is the frequency of the jth allele for marker i, ij ij ij fragments, respectively, observed between ith and jth and the summation extends over n alleles. This formula is varieties (Nei and Li 1979). The dissimilarity of each the same as for calculating the expected heterozygosity variety pair was calculated as “1-F ”. Genetic variation for a random mating population, and the polymorphism ij within rice group was examined based on their average information content (PIC) value for self-pollinating dissimilarity indices. plants. The averages were used as overall gene diversity Table 4 Number of alleles (A) and gene diversity value (B) observed for eight groups of Vietnamese local varieties Group Locus Average RM2 RM29 RM31 RM60 RM201 RM208 RM225 RM232 RM237 RM241 (Chr. 7) (Chr. 2) (Chr. 5) (Chr. 3) (Chr. 9) (Chr. 2) (Chr. 6) (Chr. 3) (Chr. 1) (Chr. 4) North Vietnam Fifth month rice A 2 2 4 2 4 3 2 6 2 8 3.5 (n=35) B 0.161 0.056 0.384 0.208 0.528 0.213 0.056 0.722 0.056 0.754 0.31 Tenth month rice A 3 1 3 2 4 4 4 7 6 7 4.1 (n=37) B 0.152 0.000 0.569 0.497 0.505 0.554 0.608 0.663 0.627 0.711 0.49 Glutinous rice N A 2 2 3 2 4 4 4 5 2 4 3.2 (n=14) B 0.426 0.459 0.592 0.444 0.582 0.582 0.604 0.722 0.426 0.556 0.54 South Vietnam Early rice A 2 2 2 2 5 5 4 3 2 7 3.4 (n=33) B 0.430 0.033 0.500 0.425 0.586 0.741 0.559 0.365 0.298 0.823 0.48 Half season rice A 1 1 4 2 4 5 3 7 4 8 3.9 (n=27) B 0.000 0.000 0.469 0.403 0.403 0.781 0.366 0.618 0.350 0.806 0.42 Season rice A 4 2 3 2 5 8 6 6 3 6 4.5 (n=53) B 0.409 0.021 0.399 0.413 0.715 0.848 0.313 0.365 0.414 0.723 0.46 Late rice A 2 1 4 2 4 4 1 3 4 4 2.9 (n=12) B 0.444 0.000 0.583 0.500 0.597 0.681 0.000 0.292 0.446 0.708 0.43 Glutinous rice S A 3 1 3 2 1 3 1 6 2 3 2.5 (n=11) B 0.512 0.000 0.562 0.320 0.000 0.579 0.000 0.810 0.496 0.645 0.39 All Vietnam A 4 2 7 2 7 10 8 14 6 12 7.2 (n=222) B 0.322 0.064 0.654 0.497 0.656 0.766 0.475 0.672 0.418 0.819 0.53 174 Rice (2011) 4:170–177 Table 5 Nei’s genetic distances Group North Vietnam South Vietnam calculated between eight Vietnamese rice groups Fifth Tenth Glu N Early Half Season Late Tenth 0.223 Glu N 0.493 0.389 Early 0.370 0.268 0.518 Half 0.340 0.248 0.554 0.135 Season 0.355 0.365 0.681 0.096 0.092 The abbreviations of the groups Late 0.385 0.515 0.926 0.166 0.216 0.080 are the same as shown in Glu S 0.433 0.510 0.986 0.223 0.280 0.154 0.127 Table 3 values to compare the genetic variation within groups and cultivated during the dry season, requires strong lodging populations. resistance before the rainy season and draught tolerance during the vegetative growth period (Hamada 1965). Evaluation of genetic differentiation among cultivated Therefore, limited genotypes might be selected for this rice and wild rice groups group. The other South Vietnamese rice groups had moderate dissimilarity values (0.41–0.45), suggesting similar Nei’s genetic distance (Nei 1972) was calculated using levels of variation within groups, although their growing/ POPGENE ver. 1.31 (Yeh et al. 1999) to measure genetic harvesting periods during the rainy season were different. differentiation among cultivated groups and wild rice Genetic variation within groups was also examined populations. The genetic distances among local variety based on gene diversity values (Table 4). The relative groups and wild populations were calculated, and unrooted average values for the eight groups were similar to the dendrograms were constructed using the UPGMA methods average dissimilarity values. and the program TreeView (Page 1996). Allelic diversity at SSR loci observed among Vietnamese local varieties Results and discussion Ten SSR markers were used to examine the genetic Evaluation of genetic variation within Vietnamese local variation among the 222 local varieties. Their allelic variety groups diversity was examined using gene diversity values, which are identical to the PIC values for self-pollinating plants. In Genetic variation within groups was studied based on the all Vietnamese varieties, the PIC values of the ten SSR dissimilarity of electromorph band patterns using 10 SSR markers ranged from 0.064 (RM29) to 0.819 (RM241), and markers. Table 3 shows the average dissimilarity values observed within Vietnamese local variety groups. The overall average dissimilarity among Vietnamese local varieties was 0.51, indicating that a pair of Vietnamese local varieties chosen randomly may share almost half of the alleles at the ten SSR loci. Among the eight groups, the highest average dissimilarity value (0.49) was observed for “Tenth month rice”. According to Hamada (1965), “Tenth month rice” can be further classified into two types. This rice group was planted in nearly 70% of all rice field in North Vietnam. These observations might explain why “Tenth month rice” maintained a high genetic diversity. Relatively higher values, 0.44 and 0.47, were observed for “Glutinous rice N” and “Glutinous rice S”, respectively. However, the overall average dissimilarity for “Glutinous rice” was 0.59, indicat- ing geographical differentiation between the two glutinous rice groups. The lowest average dissimilarity, 0.32, was Fig. 2 A phylogenic tree based on Nei’s genetic distances among eight Vietnamese rice groups. detected for “Fifth month rice”. “Fifthmonthrice”, Rice (2011) 4:170–177 175 averaged 0.53. Seven out of the ten SSR markers (all except distance between two North Vietnamese varieties (“Tenth RM60, RM201, and RM29) were previously used to month rice” and “Fifth month rice”) was 0.223, and the examine genetic diversity in 23 Asian cultivars of O. sativa highest value of 0.986 was observed between “Glutinous (Ishii et al. 2001). The average PIC values at the seven SSR rice N” and “Glutinous rice S”. A phylogenic tree was loci in this study and the previous study were 0.59 and constructed based on the genetic distance values between 0.78, respectively, suggesting that relatively high levels of all pairs (Fig. 2). Two small clusters were generated: one polymorphisms were observed among local varieties consisted of common South Vietnamese rice groups and collected from one country. “Glutinous rice S”, and the other included the North Vietnamese groups (“Tenth month rice” and “Fifth month Evaluation of genetic differentiation among Vietnamese rice”), suggesting the geographical separation of the rice rice groups groups. “Glutinous rice N” showed the widest differentia- tion from all other groups, and “Glutinous rice S” was Nei’s genetic distances were calculated between all pairs of located in the outer branch of the South Vietnamese groups. Vietnamese rice groups to examine their genetic differen- These results suggest that selection based on human tiation (Table 5). A higher value indicates greater genetic preference for rice grain characters had a great influence differentiation between the two groups. Relatively low on the diversification of glutinous rice in Vietnam. genetic distance values (0.080–0.216) were observed between common rice groups (“Early rice”, “Half season Evaluation of genetic variation within wild rice populations rice”, “Season rice”,and “Late rice”) in South Vietnam. Their close relationships might be due to the partially Leaf samples of wild rice were collected at three sites overlapping crop seasons in the same region. The genetic (PT-1, YG-23, and AK-18) in Myanmar and three (CT- Table 6 Number of alleles (A), gene diversity (B), and observed heterogenity (C) found in six wild rice populations in Myanmar and Vietnam Group Locus Average RM31 RM60 RM201 RM208 RM237 (Chr. 5) (Chr. 3) (Chr. 9) (Chr. 2) (Chr. 1) Myanmar (wild rice) PT-1 (n=180) A 12 6 10 10 21 11.8 B 0.870 0.722 0.612 0.755 0.848 0.76 C 0.678 0.682 0.154 0.697 0.805 0.60 YG-23 (n=280) A 7 4 5 4 8 5.6 B 0.522 0.590 0.307 0.407 0.679 0.50 C 0.347 0.903 0.079 0.204 0.843 0.48 AK-18 (n=156) A 10 2 4 10 7 6.6 B 0.224 0.006 0.063 0.559 0.107 0.19 C 0.118 0.006 0.064 0.077 0.072 0.07 Vietnam (wild rice) CT-61 (n=140) A 4 2 8 4 7 5.0 B 0.501 0.030 0.707 0.618 0.626 0.50 C 0.711 0.030 0.114 0.985 0.962 0.56 CT-65 (n=80) A 3 3 3 6 5 4.0 B 0.485 0.372 0.249 0.683 0.704 0.50 C 0.000 0.354 0.000 0.949 0.962 0.45 CT-67 (n=140) A 16 7 15 11 21 14.0 B 0.891 0.698 0.871 0.795 0.784 0.81 C 0.820 0.625 0.712 0.829 0.609 0.72 Vietnam (local varieties) (n=222) A 7 2 7 10 6 6.4 B 0.654 0.497 0.656 0.766 0.418 0.60 C 0.000 0.005 0.005 0.023 0.005 0.01 176 Rice (2011) 4:170–177 Table 7 Nei’s genetic distances calculated between six wild rice annual populations. This would cause low genetic varia- populations tion within a small self-pollinated population. Group Myanmar Vietnam Genetic differentiation among wild rice populations PT-1 YG-23 AK-18 CT-61 CT-65 CT-67 in Myanmar and Vietnam PT-1 – The genetic differentiation among wild rice populations in YG-23 0.318 – Myanmar and Vietnam was calculated based on the genetic AK-18 1.670 1.372 – distances between them (Table 7). Using these values, a CT-61 1.138 2.021 2.281 – phylogenic tree was constructed as shown in Fig. 3. The CT-65 1.677 3.059 2.353 0.617 – three populations each in Myanmar and Vietnam did not CT-67 0.505 0.917 1.097 0.886 0.678 – form clear geographical groups. The annual AK-18 popu- lation showed marked differentiation from the others, and the two populations at PT-1 and CT-67, with higher genetic 61, CT-65, and CT-67) in Vietnam. Based on the variation within populations, made a small cluster. These electromorph allele data, the number of alleles over results indicate that ecological factors had a much greater the five SSR loci, gene diversity (corresponding to the influence on genetic differentiation among the wild rice expected heterozygosity), and the observed heterozygos- populations than did geographical factors. ity were calculated for each population (Table 6). Among the six populations investigated, high average Comparison of genetic variation between wild rice gene diversity values were observed for the PT-1 (0.76) and local varieties and CT-67 (0.81) populations, whereas low values were calculated for AK-18 (0.19). The PT-1 and CT-67 habitats To compare the degrees of genetic variation in wild rice and were deepwater areas, and these populations were huge. local varieties, the overall number of alleles and gene No disturbance (e.g., animal grazing or human cutting) diversity were calculated for five common microsatellite was observed in the population. Therefore, the high levels loci (RM31, RM60, RM201, RM208, and RM237) in the of genetic variation might be maintained by clonal 222 Vietnamese local varieties (Table 6). The number of propagation under stable environmental conditions. By alleles ranged from two to ten, with an average of 6.4, and contrast, the wild rice plants at AK-18 were typical annual the gene diversity was 0.418–0.766, and averaged 0.60. forms, and they propagated solely through seed. The Although local cultivars were collected from various areas observed heterogeneity was quite low (0.07), indicating in Vietnam, these average values were less than those that most of the plants were fixed to homozygote forms in detected at PT-1 (11.8 for average number of alleles, and 0.76 for average gene diversity) and CT-67 (14.0, and 0.81). In particular, only 140 wild plants were surveyed at a single site of CT-67 in Vietnam, and the numbers of alleles and the gene diversity values at five loci were all higher than those in Vietnamese local varieties (Table 6). In addition, wide genetic differentiation was observed among wild rice populations in Myanmar and Vietnam (Fig. 3). These results indicate that wild rice has much higher genetic variation than cultivated rice. Acknowledgments We thank Dr. Tin Htut and Mr. Minn San Thein, Department of Agricultural Research, Myanmar, and Dr. Nguyen Thi Lang, Cuulong Delta Rice Research Institute, Vietnam, for their kind research collaboration on wild rice survey. References Cai HW, Wang XK, Morishima H. Comparison of population genetic structures of common wild rice (Oryza rufipogon Griff.), as revealed by analyses of quantitative traits, allozymes, and RFLPs. Fig. 3 A phylogenic tree based on Nei’s genetic distances among six Heredity. 2004;92:409–17. wild rice populations in Myanmar and Vietnam. Rice (2011) 4:170–177 177 Chen X, Temnykh S, Xu Y, Cho YG, McCouch SR. Development of a Song ZP, Xu X, Wang B, Chen JK, Lu BR. Genetic diversity in the microsatellite framework map providing genome-wide coverage northernmost Oryza rufipogon populations estimated by SSR in rice (Oryza sativa L.). Theor Appl Genet. 1997;95:553–67. markers. Theor Appl Genet. 2003;107:1492–9. Gao L. Population structure and conservation genetics of wild rice Sun CQ, Wang XK, Yoshimura A, Doi K. Genetic differentiation for Oryza rufipogon (Poaceae): a region-wide perspective from nuclear, mitochondrial and chloroplast genomes in common wild microsatellite variation. Mol Ecol. 2004;13:1009–24. rice (Oryza rufipogon Griff.) and cultivated rice (Oryza sativa Hamada H. Rice in Mekong valleys. In: Indo-Chinese studies, L.). Theor Appl Genet. 2002;104:1335–45. Synthetic research of the culture of rice-cultivating races in Tanksley SD, McCouch SR. Seed banks and molecular maps: unlocking Southeast Asian countries. The Japanese Society of Ethnology genetic potential from the wild. Science. 1997;277:1063–6. (Tokyo). 1965;1:507–586 Tanksley SD, Grandillo S, Fulton TM, Zamir D, Eshed Y, Petiard V, et Ishii T, Xu Y, McCouch SR. Nuclear- and chloroplast-microsatellite al. Advanced backcross QTL analysis in a cross between an elite variation in a genome species of rice. Genome. 2001;44:658–66. processing line of tomato and its wild relative L. pimpinellifo- McCouch SR, Chen X, Panaud O, Temnykh S, Xu Y, Cho YG, et al. lium. Theor Appl Genet. 1996;92:213–24. Microsatellite marker development, mapping and applications in Temnykh S, DeClerck G, Lukashova A, Lipovich L, Cartinhour S, rice genetics and breeding. Plant Mol Biol. 1997;35:89–99. McCouch SR. Computational and experimental analysis of Nei M. Genetic distance between populations. Am Nat. 1972;106:283–92. microsatellites in rice (Oryza sativa L.): frequency, length Nei M. Molecular evolutionary genetics. New York: Columbia variation, transposon associations, and genetic marker potential. University Press; 1987. Genome Res. 2001;11:1441–52. Nei M, Li WH. Mathematical model for studying genetic variation in Xiao J, Li J, Grandillo S, Ahn SN, Yuan L, Tanksley SD, et al. Genes terms of restriction endonuclease. Proc Natl Acad Sci USA. from wild rice improve yield. Nature. 1996;384:223–4. 1979;76:5269–73. Xiao J, Li J, Grandillo S, Ahn SN, Yuan L, Tanksley SD, et al. Oka H. The ancestors of cultivate rice. In: Origin of cultivated rice. Identification of trait-improving quantitative trait loci alleles from a Tokyo: Japan Scientific Societies Press; 1988. p. 15–24 wild rice relative, Oryza rufipogon. Genetics. 1998;150:899–909. Page RDM. TREEVIEW: an application to display phylogenic trees Yeh FC, Yang RC, Boyle T. POPGENE. 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Evaluation of Genetic Variation Among Wild Populations and Local Varieties of Rice

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Springer Journals
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Copyright © 2011 by Springer Science+Business Media, LLC
Subject
Life Sciences; Plant Sciences; Plant Genetics & Genomics; Plant Breeding/Biotechnology; Agriculture; Plant Ecology
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1939-8425
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1939-8433
DOI
10.1007/s12284-011-9067-x
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Abstract

Rice (2011) 4:170–177 DOI 10.1007/s12284-011-9067-x Evaluation of Genetic Variation Among Wild Populations and Local Varieties of Rice Takashige Ishii & Takashi Hiraoka & Tomoyuki Kanzaki & Masahiro Akimoto & Rieko Shishido & Ryo Ishikawa Received: 21 October 2011 /Accepted: 1 November 2011 /Published online: 19 November 2011 Springer Science+Business Media, LLC 2011 Abstract Cultivated rice (Oryza sativa L.) is derived from Introduction Asian wild rice (Oryza rufipogon Griff). Vietnamese local varieties and wild natural populations in Vietnam and Most crop species were originally derived from wild Myanmar were examined to evaluate the levels of genetic species. In the early days of domestication, primitive variation in cultivated and wild rice. In total, 222 Vietnamese farmers may have unconsciously chosen desirable plants local varieties were analyzed with ten microsatellite markers. based on several simple traits related to shattering habit, Using marker genotype and gene diversity data, the local seed dormancy, and seed size. However, the domestication varieties were differentiated based on geographical distribu- and selection process led to a rapid reduction in the genetic tion, cropping season, and human preference. A total of 976 diversity of crop species (Tanksley and McCouch 1997). wild plants were collected at six natural sites of wild Wild species maintain many genes that have been lost populations (three each in Myanmar and Vietnam), and the during domestication. Among them, trait-improving quan- degrees of variation among populations were analyzed with titative trait loci from wild relatives have been identified in five microsatellite markers. Phylogenetic analyses revealed various crops (Xiao et al. 1996, 1998; Tanksley et al. 1996). wide genetic differentiation among wild populations. The Such studies suggest that wild species still maintain many diversity values detected in a single wild population in beneficial alleles for future plant breeding. Vietnam were higher than those in whole Vietnamese local Oryza rufipogon is the ancestral wild species of varieties. These results indicate that wild rice has much cultivated rice, Oryza sativa (Oka 1988). They share the greater genetic variation than cultivated rice. same AA genome and show high levels of cross compat- ibility. Therefore, O. rufipogon may be the most important . . . Keywords Genetic variation Rice Local variety Wild wild genetic resource for rice breeding programs, because rice (Oryza rufipogon) its useful genes can be easily transferred by crossing. Although cultivated rice has less genetic variation than wild rice, local varieties have maintained many useful traits. : : : T. Ishii (*) T. Hiraoka T. Kanzaki R. Ishikawa Local varieties are cultivated forms developed by adapta- Graduate School of Agricultural Science, Kobe University, tion to the natural and cultural environment in each area Rokkodai, Nada-ku, and are more genetically diverse than modern breeding Kobe 657-8501, Japan e-mail: tishii@kobe-u.ac.jp varieties. Molecular markers have become powerful tools for M. Akimoto investigating genetic diversity among crop species. In Obihiro University of Agriculture and Veterinary Medicine, particular, microsatellite or simple sequence repeat (SSR) Inada, Obihiro 080-8555, Japan markers are useful for revealing intra- and inter-specific variation because they are codominant with high levels of R. Shishido allelic diversity (McCouch et al. 1997). Microsatellites are College of Bioresource Science, Nihon University, tandemly arranged repeats of short DNA motifs (1–4bpin Kameino, length) that frequently exhibit variation in the number of Fujisawa 252-8510, Japan Rice (2011) 4:170–177 171 repeats at a locus (Temnykh et al. 2001). Therefore, we and South Vietnam. According to the report, North Vietnam used microsatellite markers to evaluate genetic variation in local varieties were classified into two groups, “Fifth month rice. rice” and “Tenth month rice”. The former was grown First, we analyzed 222 local varieties originated from during the dry season, whereas the latter during rainy various areas in Vietnam. They were collected more than season. South Vietnam local varieties were divided into 50 years ago by the late Prof. Hamada, Hyogo University several groups based on the growing period during the of Agriculture, Japan, during a scientific expedition to rainy season and seed characters (“Early rice”, “Half season Indo-China. They are suitable materials for analyzing rice”, “Season rice”, “Late rice”, and “Glutinous rice”). genetic variation among local varieties before introducing Hamada (1965) classified “Glutinous rice” as South modern breeding methodologies. As for wild species of O. Vietnam varieties; however, half of them came from North rufipogon, many studies have been conducted to reveal the Vietnam according to the collection sites. Therefore, in this genetic differentiation among Asian accessions (Ishii et al. study, “Glutinous rice” was further divided into two groups, 2001; Sun et al. 2002; Cai et al. 2004). They usually used “Glutinous rice N” and “Glutinous rice S” for North and seed/plant materials derived from wild rice accessions South Vietnam, respectively. maintained in germplasm institutes or seed banks, but these accessions do not represent the features of natural wild rice. DNA extraction Wild natural populations in southern China were investi- gated by several research groups (Song et al. 2003; Zhou et Total DNA of the local variety was extracted from seed al. 2003;Gao 2004); however, those in the major specimen. For each variety, the embryo segment was distribution area of O. rufipogon have never been analyzed removed from a single seed and ground in 100 μlof in detail. In this study, a large-scale survey on wild rice was extracting solution containing 20 mM Tris–HCl (pH 8.0), carried out using 976 individuals from six natural popula- 5 mM EDTA, 400 mM NaCl, 0.3% SDS, and 200 μg/ml tions in Myanmar and Vietnam, and genetic variation proteinase K. The supernatant was used directly as the among wild rice populations was evaluated. In addition, template for PCR. the degree of genetic variation in wild rice was compared with that in local varieties. Research sites for the wild rice populations Research trips to collect wild rice were made to Myanmar Materials and methods in 2008 and Vietnam in 2007. Based on various population factors, such as ecotype (annual or perennial), size and Local varieties degree of disturbance, three research sites each in Myanmar (PT-1, YG-23, and AK-18) and Vietnam (CT-61, CT-65, In total, 222 Vietnamese local rice varieties were used and CT-67) were established for wild rice observations (Table 1). They were collected by the late Prof. Hamada, (Fig. 1). Environmental and geographical information for Hyogo University of Agriculture, in 1957 and 1958. Their these six observation sites is shown in Table 2. origins and ecological characteristics were described in a research report titled “Rice in Mekong Valleys” by Hamada Wild rice sample collection (1965). At the time of collection, Vietnam comprised North At each site, leaves were collected from the different plants Table 1 Vietnamese local varieties used in this study at 1–4-m intervals according to population size. In total, 976 wild natural plants from the six sites in Myanmar and Region Group Number of varieties Vietnam were surveyed. The number of samples ranged from 80 (CT-65) to 280 (YG-23), with an average of 162.6 North Fifth month rice 35 (Table 2). The collected leaf samples were crushed with a Tenth month rice 37 wooden hammer, and the leaf extract was fixed on an FTA Glutinous rice N 14 card (GE Healthcare). Samples were brought back to the South Early rice 33 laboratory, and small discs that were punched out from the Half season rice 27 FTA cards were used directly as PCR templates. Season rice 53 Late rice 12 Polymorphism detection using SSR markers Glutinous rice S 11 Total 222 Ten SSR markers (RM2, RM29, RM31, RM60, RM201, Classified by Hamada (1965) RM208, RM225, RM232, RM237, and RM241) were used. 172 Rice (2011) 4:170–177 Fig. 1 Geographical location of the wild rice populations studied in Myanmar and Vietnam. Of these, RM29 and RM208 are located on chromosome 2, 0.5 U of NovaTaq (Shimadzu, Japan). Amplification was and RM60 and RM232 on chromosomes 3. However, they performed with an MP Thermal Cycler (TaKaRa Bio, are not linked because their map distances are much more Japan) as follows: 94°C for 5 min, followed by 35 cycles of than 50 cM (Chen et al. 1997). Five SSR markers (RM31, 94°C for 1 min, 55°C for 1 min, 72°C for 2 min, and RM60, RM201, RM208, and RM237) were used for the ending with 5 min at 72°C for the final extension. The wild rice survey. PCR was performed in a 10–15 μl mixture amplified products were electrophoresed on 4% polyacryl- containing 1 μM of each primer, a half volume of 2× amide gels, and the banding pattern was visualized using a Ampdirect plus buffer (Shimadzu, Japan), 1 μl of template non-radioactive silver staining method, as described by DNA (or a small disc punched out from the FTA card), and Panaud et al. (1996). Table 2 Site information on wild rice populations in Myanmar and Vietnam Site Ecotype Population size Habitat Number of samples Latitude Longitude Myanmar PT-1 Perennial >3 km Deep water 180 17°03′52.5″ 95°35′20.3″ YG-23 Perennial c.a. 200 m Road-side swamp 280 17°08′49.1″ 96°17′28.4″ AK-18 Annual c.a. 150 m Paddy side 156 20°15′02.7″ 92°49′13.9″ Vietnam CT-61 Perennial c.a. 250 m Orange farm ditch 140 10°20′45.8″ 105°56′06.7″ CT-65 Perennial c.a. 3 km Canal (discontinuous) 80 09°46′48.9″ 105°38′02.9″ CT-67 Perennial c.a. 1.5 km Deep water 140 10°42′43.8″ 105°30′16.1″ Rice (2011) 4:170–177 173 Table 3 Average dissimilarity values within Vietnamese local variety groups Group North Vietnam South Vietnam Overall Fifth Tenth Glu N Early Half Season Late Glu S means Average dissimilarity 0.32 0.49 0.44 0.45 0.41 0.42 0.41 0.47 0.51 Fifth Fifth month rice, Tenth Tenth month rice, Early Early rice, Half Half season rice, Season Season rice, Late Late rice, Glu N Glutinous N, Glu S Glutinous S Evaluation of genetic variation within local variety groups Cultivated rice is a self-pollinating crop, whereas wild and wild populations ancestral O. rufipogon is cross-pollinating. Therefore, genetic variation within groups (or populations) was also Genetic variation within local variety groups was studied examined based on gene diversity, which can be applied to based on the dissimilarity of SSR electromorph allele sizes. plants with any pollinating system (Nei 1987). The gene The ratio of common fragments was calculated as a diversity values were calculated as follows: similarity index according to the following formula: H ¼ 1  x i ij F ¼ 2B =A j¼1 ij ij ij where A and B are the number of total and common where x is the frequency of the jth allele for marker i, ij ij ij fragments, respectively, observed between ith and jth and the summation extends over n alleles. This formula is varieties (Nei and Li 1979). The dissimilarity of each the same as for calculating the expected heterozygosity variety pair was calculated as “1-F ”. Genetic variation for a random mating population, and the polymorphism ij within rice group was examined based on their average information content (PIC) value for self-pollinating dissimilarity indices. plants. The averages were used as overall gene diversity Table 4 Number of alleles (A) and gene diversity value (B) observed for eight groups of Vietnamese local varieties Group Locus Average RM2 RM29 RM31 RM60 RM201 RM208 RM225 RM232 RM237 RM241 (Chr. 7) (Chr. 2) (Chr. 5) (Chr. 3) (Chr. 9) (Chr. 2) (Chr. 6) (Chr. 3) (Chr. 1) (Chr. 4) North Vietnam Fifth month rice A 2 2 4 2 4 3 2 6 2 8 3.5 (n=35) B 0.161 0.056 0.384 0.208 0.528 0.213 0.056 0.722 0.056 0.754 0.31 Tenth month rice A 3 1 3 2 4 4 4 7 6 7 4.1 (n=37) B 0.152 0.000 0.569 0.497 0.505 0.554 0.608 0.663 0.627 0.711 0.49 Glutinous rice N A 2 2 3 2 4 4 4 5 2 4 3.2 (n=14) B 0.426 0.459 0.592 0.444 0.582 0.582 0.604 0.722 0.426 0.556 0.54 South Vietnam Early rice A 2 2 2 2 5 5 4 3 2 7 3.4 (n=33) B 0.430 0.033 0.500 0.425 0.586 0.741 0.559 0.365 0.298 0.823 0.48 Half season rice A 1 1 4 2 4 5 3 7 4 8 3.9 (n=27) B 0.000 0.000 0.469 0.403 0.403 0.781 0.366 0.618 0.350 0.806 0.42 Season rice A 4 2 3 2 5 8 6 6 3 6 4.5 (n=53) B 0.409 0.021 0.399 0.413 0.715 0.848 0.313 0.365 0.414 0.723 0.46 Late rice A 2 1 4 2 4 4 1 3 4 4 2.9 (n=12) B 0.444 0.000 0.583 0.500 0.597 0.681 0.000 0.292 0.446 0.708 0.43 Glutinous rice S A 3 1 3 2 1 3 1 6 2 3 2.5 (n=11) B 0.512 0.000 0.562 0.320 0.000 0.579 0.000 0.810 0.496 0.645 0.39 All Vietnam A 4 2 7 2 7 10 8 14 6 12 7.2 (n=222) B 0.322 0.064 0.654 0.497 0.656 0.766 0.475 0.672 0.418 0.819 0.53 174 Rice (2011) 4:170–177 Table 5 Nei’s genetic distances Group North Vietnam South Vietnam calculated between eight Vietnamese rice groups Fifth Tenth Glu N Early Half Season Late Tenth 0.223 Glu N 0.493 0.389 Early 0.370 0.268 0.518 Half 0.340 0.248 0.554 0.135 Season 0.355 0.365 0.681 0.096 0.092 The abbreviations of the groups Late 0.385 0.515 0.926 0.166 0.216 0.080 are the same as shown in Glu S 0.433 0.510 0.986 0.223 0.280 0.154 0.127 Table 3 values to compare the genetic variation within groups and cultivated during the dry season, requires strong lodging populations. resistance before the rainy season and draught tolerance during the vegetative growth period (Hamada 1965). Evaluation of genetic differentiation among cultivated Therefore, limited genotypes might be selected for this rice and wild rice groups group. The other South Vietnamese rice groups had moderate dissimilarity values (0.41–0.45), suggesting similar Nei’s genetic distance (Nei 1972) was calculated using levels of variation within groups, although their growing/ POPGENE ver. 1.31 (Yeh et al. 1999) to measure genetic harvesting periods during the rainy season were different. differentiation among cultivated groups and wild rice Genetic variation within groups was also examined populations. The genetic distances among local variety based on gene diversity values (Table 4). The relative groups and wild populations were calculated, and unrooted average values for the eight groups were similar to the dendrograms were constructed using the UPGMA methods average dissimilarity values. and the program TreeView (Page 1996). Allelic diversity at SSR loci observed among Vietnamese local varieties Results and discussion Ten SSR markers were used to examine the genetic Evaluation of genetic variation within Vietnamese local variation among the 222 local varieties. Their allelic variety groups diversity was examined using gene diversity values, which are identical to the PIC values for self-pollinating plants. In Genetic variation within groups was studied based on the all Vietnamese varieties, the PIC values of the ten SSR dissimilarity of electromorph band patterns using 10 SSR markers ranged from 0.064 (RM29) to 0.819 (RM241), and markers. Table 3 shows the average dissimilarity values observed within Vietnamese local variety groups. The overall average dissimilarity among Vietnamese local varieties was 0.51, indicating that a pair of Vietnamese local varieties chosen randomly may share almost half of the alleles at the ten SSR loci. Among the eight groups, the highest average dissimilarity value (0.49) was observed for “Tenth month rice”. According to Hamada (1965), “Tenth month rice” can be further classified into two types. This rice group was planted in nearly 70% of all rice field in North Vietnam. These observations might explain why “Tenth month rice” maintained a high genetic diversity. Relatively higher values, 0.44 and 0.47, were observed for “Glutinous rice N” and “Glutinous rice S”, respectively. However, the overall average dissimilarity for “Glutinous rice” was 0.59, indicat- ing geographical differentiation between the two glutinous rice groups. The lowest average dissimilarity, 0.32, was Fig. 2 A phylogenic tree based on Nei’s genetic distances among eight Vietnamese rice groups. detected for “Fifth month rice”. “Fifthmonthrice”, Rice (2011) 4:170–177 175 averaged 0.53. Seven out of the ten SSR markers (all except distance between two North Vietnamese varieties (“Tenth RM60, RM201, and RM29) were previously used to month rice” and “Fifth month rice”) was 0.223, and the examine genetic diversity in 23 Asian cultivars of O. sativa highest value of 0.986 was observed between “Glutinous (Ishii et al. 2001). The average PIC values at the seven SSR rice N” and “Glutinous rice S”. A phylogenic tree was loci in this study and the previous study were 0.59 and constructed based on the genetic distance values between 0.78, respectively, suggesting that relatively high levels of all pairs (Fig. 2). Two small clusters were generated: one polymorphisms were observed among local varieties consisted of common South Vietnamese rice groups and collected from one country. “Glutinous rice S”, and the other included the North Vietnamese groups (“Tenth month rice” and “Fifth month Evaluation of genetic differentiation among Vietnamese rice”), suggesting the geographical separation of the rice rice groups groups. “Glutinous rice N” showed the widest differentia- tion from all other groups, and “Glutinous rice S” was Nei’s genetic distances were calculated between all pairs of located in the outer branch of the South Vietnamese groups. Vietnamese rice groups to examine their genetic differen- These results suggest that selection based on human tiation (Table 5). A higher value indicates greater genetic preference for rice grain characters had a great influence differentiation between the two groups. Relatively low on the diversification of glutinous rice in Vietnam. genetic distance values (0.080–0.216) were observed between common rice groups (“Early rice”, “Half season Evaluation of genetic variation within wild rice populations rice”, “Season rice”,and “Late rice”) in South Vietnam. Their close relationships might be due to the partially Leaf samples of wild rice were collected at three sites overlapping crop seasons in the same region. The genetic (PT-1, YG-23, and AK-18) in Myanmar and three (CT- Table 6 Number of alleles (A), gene diversity (B), and observed heterogenity (C) found in six wild rice populations in Myanmar and Vietnam Group Locus Average RM31 RM60 RM201 RM208 RM237 (Chr. 5) (Chr. 3) (Chr. 9) (Chr. 2) (Chr. 1) Myanmar (wild rice) PT-1 (n=180) A 12 6 10 10 21 11.8 B 0.870 0.722 0.612 0.755 0.848 0.76 C 0.678 0.682 0.154 0.697 0.805 0.60 YG-23 (n=280) A 7 4 5 4 8 5.6 B 0.522 0.590 0.307 0.407 0.679 0.50 C 0.347 0.903 0.079 0.204 0.843 0.48 AK-18 (n=156) A 10 2 4 10 7 6.6 B 0.224 0.006 0.063 0.559 0.107 0.19 C 0.118 0.006 0.064 0.077 0.072 0.07 Vietnam (wild rice) CT-61 (n=140) A 4 2 8 4 7 5.0 B 0.501 0.030 0.707 0.618 0.626 0.50 C 0.711 0.030 0.114 0.985 0.962 0.56 CT-65 (n=80) A 3 3 3 6 5 4.0 B 0.485 0.372 0.249 0.683 0.704 0.50 C 0.000 0.354 0.000 0.949 0.962 0.45 CT-67 (n=140) A 16 7 15 11 21 14.0 B 0.891 0.698 0.871 0.795 0.784 0.81 C 0.820 0.625 0.712 0.829 0.609 0.72 Vietnam (local varieties) (n=222) A 7 2 7 10 6 6.4 B 0.654 0.497 0.656 0.766 0.418 0.60 C 0.000 0.005 0.005 0.023 0.005 0.01 176 Rice (2011) 4:170–177 Table 7 Nei’s genetic distances calculated between six wild rice annual populations. This would cause low genetic varia- populations tion within a small self-pollinated population. Group Myanmar Vietnam Genetic differentiation among wild rice populations PT-1 YG-23 AK-18 CT-61 CT-65 CT-67 in Myanmar and Vietnam PT-1 – The genetic differentiation among wild rice populations in YG-23 0.318 – Myanmar and Vietnam was calculated based on the genetic AK-18 1.670 1.372 – distances between them (Table 7). Using these values, a CT-61 1.138 2.021 2.281 – phylogenic tree was constructed as shown in Fig. 3. The CT-65 1.677 3.059 2.353 0.617 – three populations each in Myanmar and Vietnam did not CT-67 0.505 0.917 1.097 0.886 0.678 – form clear geographical groups. The annual AK-18 popu- lation showed marked differentiation from the others, and the two populations at PT-1 and CT-67, with higher genetic 61, CT-65, and CT-67) in Vietnam. Based on the variation within populations, made a small cluster. These electromorph allele data, the number of alleles over results indicate that ecological factors had a much greater the five SSR loci, gene diversity (corresponding to the influence on genetic differentiation among the wild rice expected heterozygosity), and the observed heterozygos- populations than did geographical factors. ity were calculated for each population (Table 6). Among the six populations investigated, high average Comparison of genetic variation between wild rice gene diversity values were observed for the PT-1 (0.76) and local varieties and CT-67 (0.81) populations, whereas low values were calculated for AK-18 (0.19). The PT-1 and CT-67 habitats To compare the degrees of genetic variation in wild rice and were deepwater areas, and these populations were huge. local varieties, the overall number of alleles and gene No disturbance (e.g., animal grazing or human cutting) diversity were calculated for five common microsatellite was observed in the population. Therefore, the high levels loci (RM31, RM60, RM201, RM208, and RM237) in the of genetic variation might be maintained by clonal 222 Vietnamese local varieties (Table 6). The number of propagation under stable environmental conditions. By alleles ranged from two to ten, with an average of 6.4, and contrast, the wild rice plants at AK-18 were typical annual the gene diversity was 0.418–0.766, and averaged 0.60. forms, and they propagated solely through seed. The Although local cultivars were collected from various areas observed heterogeneity was quite low (0.07), indicating in Vietnam, these average values were less than those that most of the plants were fixed to homozygote forms in detected at PT-1 (11.8 for average number of alleles, and 0.76 for average gene diversity) and CT-67 (14.0, and 0.81). In particular, only 140 wild plants were surveyed at a single site of CT-67 in Vietnam, and the numbers of alleles and the gene diversity values at five loci were all higher than those in Vietnamese local varieties (Table 6). In addition, wide genetic differentiation was observed among wild rice populations in Myanmar and Vietnam (Fig. 3). These results indicate that wild rice has much higher genetic variation than cultivated rice. Acknowledgments We thank Dr. Tin Htut and Mr. Minn San Thein, Department of Agricultural Research, Myanmar, and Dr. Nguyen Thi Lang, Cuulong Delta Rice Research Institute, Vietnam, for their kind research collaboration on wild rice survey. References Cai HW, Wang XK, Morishima H. Comparison of population genetic structures of common wild rice (Oryza rufipogon Griff.), as revealed by analyses of quantitative traits, allozymes, and RFLPs. 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Published: Nov 19, 2011

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