During the last 90 years, the breeding of rice has delivered cultivars with improved agronomic and economic characteristics. Crossing of different lines and successive artificial selection of progeny based on their phenotypes have changed the chromosomal constitution of the ancestors of modern rice; however, the nature of these changes is unclear. The recent accumulation of data for genome-wide single-nucleotide polymorphisms (SNPs) in rice has allowed us to investigate the change in haplotype structure and composition. To assess the impact of these changes during modern breeding, we studied 177 Japanese rice accessions, which were categorized into three groups: landraces, improved cultivars developed from 1931 to 1974 (the early breeding phase), and improved cultivars developed from 1975 to 2005 (the late breeding phase). Phylogenetic tree and structure analysis indicated genetic differentiation between non-irrigated (upland) and irrigated (lowland) rice groups as well as genetic structuring within the irrigated rice group that corresponded to the existence of three subgroups. Pedigree analysis revealed that a limited number of landraces and cultivars was used for breeding at the beginning of the period of systematic breeding and that 11 landraces accounted for 70% of the ancestors of the modern improved cultivars. The values for linkage disequilibrium estimated from SNP alleles and the haplotype diversity determined from consecutive alleles in five-SNP windows indicated that haplotype blocks became less diverse over time as a result of the breeding process. A decrease in haplotype diversity, caused by a reduced number of polymorphisms in the haplotype blocks, was observed in several chromosomal regions. However, our results also indicate that new haplotype polymorphisms have been generated across the genome during the breeding process. These findings will facilitate our understanding of the association between particular haplotypes and desirable phenotypes in modern Japanese rice cultivars.
References
[1]
Hargrove TR, Cabanilla VL (1979) Impact of semi-dwarf varieties on Asian rice-breeding programs. Bioscience 29: 731–735.
[2]
Peng S, Laza RC, Visperas RM, Sanico AL, Cassman KG, et al. (2000) Grain yield of rice cultivars and lines developed in the Philippines since 1966. Crop Sci 40: 307–314.
[3]
Horie T, Shiraiwa T, Homma K, Katsura K, Maeda S, et al. (2005) Can yields of lowland rice resume the increases that they showed in the 1980s? Plant Prod Sci 8: 259–274.
[4]
Yamamoto T, Nagasaki H, Yonemaru JI, Ebana K, Nakajima M, et al. (2010) Fine definition of the pedigree haplotypes of closely related rice cultivars by means of genome-wide discovery of single-nucleotide polymorphisms. BMC Genomics 11: 267.
[5]
Yamasaki M, Wright SI, McMullen MD (2007) Genomic screening for artificial selection during domestication and improvement in maize. Ann Bot 100: 967–973.
[6]
McNally KL, Childs KL, Bohnert R, Davidson RM, Zhao K, et al. (2009) Genomewide SNP variation reveals relationships among landraces and modern varieties of rice. Proc Natl Acad Sci U S A 106: 12273–12278.
[7]
Zhao K, Wright M, Kimball J, Eizenga G, McClung A, et al. (2010) Genomic diversity and introgression in O. sativa reveal the impact of domestication and breeding on the rice genome. PLoS One 5: e10780.
[8]
Ebana K, Yonemaru JI, Fukuoka S, Iwata H, Kanamori H, et al. (2010) Genetic structure revealed by a whole-genome single-nucleotide polymorphism survey of diverse accessions of cultivated Asian rice (Oryza sativa L.). Breed Sci 60: 390–397.
[9]
Wang L, Wang A, Huang X, Zhao Q, Dong G, et al. (2011) Mapping 49 quantitative trait loci at high resolution through sequencing-based genotyping of rice recombinant inbred lines. Theor Appl Genet 122: 327–340.
[10]
Huang X, Wei X, Sang T, Zhao Q, Feng Q, et al. (2010) Genome-wide association studies of 14 agronomic traits in rice landraces. Nat Genet 42: 961–967.
[11]
Huang X, Feng Q, Qian Q, Zhao Q, Wang L, et al. (2009) High-throughput genotyping by whole-genome resequencing. Genome Res 19: 1068–1076.
[12]
Zhang Q, Maroof MAS, Lu TY, Shen BZ (1992) Genetic diversity and differentiation of indica and japonica rice detected by RFLP analysis. Theor Appl Genet 83: 495–499.
[13]
Kono I, Takeuchi Y, Shimano T, Sasaki T, Yano M (2000) Comparison of efficiency of detecting polymorphism among japonica varieties in rice using RFLP, RAPD, AFLP and SSR markers. Breeding Res 2: 197–203. (in Japanese with English summary).
[14]
Nagasaki H, Ebana K, Shibaya T, Yonemaru Ji, Yano M (2010) Core single-nucleotide polymorphisms - a tool for genetic analysis of the Japanese rice population. Breed Sci 60: 648–655.
[15]
Arai-Kichise Y, Shiwa Y, Nagasaki H, Ebana K, Yoshikawa H, et al. (2011) Discovery of genome-wide DNA polymorphisms in a landrace cultivar of japonica rice by whole-genome sequencing. Plant Cell Physiol 52: 274–282.
[16]
Gao H, Williamson S, Bustamante CD (2007) A Markov chain Monte Carlo approach for joint inference of population structure and inbreeding rates from multilocus genotype data. Genetics 176: 1635–1651.
[17]
Yonemaru Ji, Yamamoto T, Fukuoka S, Uga Y, Hori K, et al. (2010) Q-TARO: QTL annotation rice online database. Rice 3: 194–203.
[18]
Yamamoto T, Yonemaru J, Yano M (2009) Towards the understanding of complex traits in rice: Substantially or Superficially? DNA Res 16: 141–154.
[19]
Feng L, Wang K, Li Y, Tan Y, Kong J, et al. (2007) Overexpression of SBPase enhances photosynthesis against high temperature stress in transgenic rice plants. Plant Cell Rep 26: 1635–1646.
[20]
Fukuda A, Nakamura A, Tagiri A, Tanaka H, Miyao A, et al. (2004) Function, intracellular localization and the importance in salt tolerance of a vacuolar Na(+)/H(+) antiporter from rice. Plant Cell Physiol 45: 146–159.
[21]
Furukawa T, Maekawa M, Oki T, Suda I, Iida S, et al. (2007) The Rc and Rd genes are involved in proanthocyanidin synthesis in rice pericarp. Plant J 49: 91–102.
Kang H-G, Park S, Matsuoka M, An G (2005) White-core endosperm floury endosperm-4 in rice is generated by knockout mutations in the C4-type pyruvate orthophosphate dikinase gene (OsPPDKB). Plant J 42: 901–911.
[24]
Kong Z, Li M, Yang W, Xu W, Xue Y (2006) A novel nuclear-localized CCCH-type zinc finger protein, OsDOS, is involved in delaying leaf senescence in rice. Plant Physiol 141: 1376–1388.
[25]
Kusaba M, Ito H, Morita R, Iida S, Sato Y, et al. (2007) Rice NON-YELLOW COLORING1 is involved in light-harvesting complex II and grana degradation during leaf senescence. Plant Cell 19: 1362–1375.
[26]
Lee S-K, Hwang S-K, Han M, Eom J-S, Kang H-G, et al. (2007) Identification of the ADP-glucose pyrophosphorylase isoforms essential for starch synthesis in the leaf and seed endosperm of rice (Oryza sativa L.). Plant Mol Biol 65: 531–546.
[27]
Matsui H, Miyao A, Takahashi A, Hirochika H (2010) Pdk1 kinase regulates basal disease resistance through the OsOxi1-OsPti1a phosphorylation cascade in rice. Plant Cell Physiol 51: 2082–2091.
[28]
Monna L, Kitazawa N, Yoshino R, Suzuki J, Masuda H, et al. (2002) Positional cloning of rice semidwarfing gene, sd-1: rice “Green Revolution Gene” encodes a mutant enzyme involved in gibberellin synthesis. DNA Res 9: 11–17.
[29]
Morita R, Sato Y, Masuda Y, Nishimura M, Kusaba M (2009) Defect in non-yellow coloring 3, an α/β hydrolase-fold family protein, causes a stay-green phenotype during leaf senescence in rice. Plant J 59: 940–952.
[30]
Ogo Y, Kobayashi T, Nakanishi Itai R, Nakanishi H, Kakei Y, et al. (2008) A novel NAC transcription factor, IDEF2, that recognizes the iron deficiency-responsive element 2 regulates the genes involved in iron homeostasis in plants. J Biol Chem 283: 13407–13417.
[31]
Ono E, Wong HL, Kawasaki T, Hasegawa M, Kodama O, et al. (2001) Essential role of the small GTPase Rac in disease resistance of rice. Proc Natl Acad Sci U S A 98: 759–764.
[32]
Sasaki A, Ashikari M, Ueguchi-Tanaka M, Itoh H, Nishimura A, et al. (2002) Green revolution: a mutant gibberellin-synthesis gene in rice. Nature 416: 701–702.
[33]
Sazuka T, Aichi I, Kawai T, Matsuo N, Kitano H, et al. (2005) The rice mutant dwarf bamboo shoot 1: a leaky mutant of the NACK-type kinesin-like gene can initiate organ primordia but not organ development. Plant Cell Physiol 46: 1934–1943.
[34]
Song S-Y, Chen Y, Chen J, Dai X-Y, Zhang W-H (2011) Physiological mechanisms underlying OsNAC5-dependent tolerance of rice plants to abiotic stress. Planta 1–15.
[35]
Ueguchi-Tanaka M, Ashikari M, Nakajima M, Itoh H, Katoh E, et al. (2005) GIBBERELLIN INSENSITIVE DWARF1 encodes a soluble receptor for gibberellin. Nature 437: 693–698.
[36]
Xie K, Wu C, Xiong L (2006) Genomic organization, differential expression, and interaction of SQUAMOSA promoter-binding-like transcription factors and microRNA156 in rice. Plant Physiol 142: 280–293.
[37]
Yano M, Katayose Y, Ashikari M, Yamanouchi U, Monna L, et al. (2000) Hd1, a major photoperiod sensitivity quantitative trait locus in rice, is closely related to the Arabidopsis flowering time gene CONSTANS. Plant Cell 12: 2473–2484.
[38]
Zhou J, Jiao F, Wu Z, Li Y, Wang X, et al. (2008) OsPHR2 is involved in phosphate-starvation signaling and excessive phosphate accumulation in shoots of plants. Plant Physiol 146: 1673–1686.
[39]
Zhu Q-H, Hoque M, Dennis E, Upadhyaya N (2003) Ds tagging of BRANCHED FLORETLESS 1 (BFL1) that mediates the transition from spikelet to floret meristem in rice (Oryza sativa L). BMC Plant Biology 3: 6.
[40]
International Rice Genome Sequencing Project (2005) The map-based sequence of the rice genome. Nature 436: 793–800.
[41]
Mather KA, Caicedo AL, Polato NR, Olsen KM, McCouch S, et al. (2007) The extent of linkage disequilibrium in rice (Oryza sativa L.). Genetics 177: 2223–2232.
[42]
Agrama H, Eizenga G (2008) Molecular diversity and genome-wide linkage disequilibrium patterns in a worldwide collection of Oryza sativa and its wild relatives. Euphytica 160: 339–355.
[43]
Jin L, Lu Y, Xiao P, Sun M, Corke H, et al. (2010) Genetic diversity and population structure of a diverse set of rice germplasm for association mapping. Theor Appl Genet 121: 475–487.
[44]
Ashikari M, Sasaki A, Ueguchi-Tanaka M, Itoh H, Nishimura A, et al. (2002) Loss-of-function of a rice gibberellin biosynthetic gene, GA20 oxidase (GA20ox-2), led to the rice ‘Green Revolution’. Breed Sci 52: 143–150.
[45]
Asano K, Takashi T, Miura K, Qian Q, Kitano H, et al. (2007) Genetic and molecular analysis of utility of sd1 alleles in rice breeding. Breed Sci 57: 53–58.
[46]
Asano K, Yamasaki M, Takuno S, Miura K, Katagiri S, et al. (2011) Artificial selection for a green revolution gene during japonica rice domestication. Proc Natl Acad Sci U S A 108: 11034–11039.
[47]
Takahashi Y, Teshima KM, Yokoi S, Innan H, Shimamoto K (2009) Variations in Hd1 proteins, Hd3a promoters, and Ehd1 expression levels contribute to diversity of flowering time in cultivated rice. Proc Natl Acad Sci U S A 106: 4555–4560.
[48]
Lin HX, Yamamoto T, Sasaki T, Yano M (2000) Characterization and detection of epistatic interactions of 3 QTLs, Hd1, Hd2, and Hd3, controlling heading date in rice using nearly isogenic lines. Theor Appl Genet 101: 1021–1028.
[49]
Lin H, Liang Z-W, Sasaki T, Yano M (2003) Fine mapping and characterization of quantitative trait loci Hd4 and Hd5 controlling heading date in rice. Breed Sci 53: 51–59.
[50]
Uga Y, Nonoue Y, Liang ZW, Lin HX, Yamamoto S, et al. (2007) Accumulation of additive effects generates a strong photoperiod sensitivity in the extremely late-heading rice cultivar ‘Nona Bokra’. Theor Appl Genet 114: 1457–1466.
[51]
Yamamoto T, Lin H, Sasaki T, Yano M (2000) Identification of heading date quantitative trait locus Hd6 and characterization of its epistatic interactions with Hd2 in rice using advanced backcross progeny. Genetics 154: 885–891.
[52]
Ebana K, Shibaya T, Wu J, Matsubara K, Kanamori H, et al. (2011) Uncovering of major genetic factors generating naturally occurring variation in heading date among Asian rice cultivars. Theor Appl Genet 122: 1199–1210.
[53]
Fujino K, Wu J, Sekiguchi H, Ito T, Izawa T, et al. (2010) Multiple introgression events surrounding the Hd1 flowering-time gene in cultivated rice, Oryza sativa L. Mol Genet Genomics 284: 137–146.
[54]
Yamamoto R (1992) Transition and prospects of rice breeding.;. In: Kushibuchi K, editor. Tokyo: Nogyo Gijyutsu Kyokai. pp. 1–33.
[55]
Perrier X, Jacquemoud-Collet JP (2006) DARwin software http://darwin.cirad.fr/darwin.
[56]
Devlin B, Risch N (1995) A comparison of linkage disequilibrium measures for fine-scale mapping. Genomics 29: 311–322.
[57]
Hill WG, Weir BS (1994) Maximum-likelihood estimation of gene location by linkage disequilibrium. Am J Hum Genet 54: 705–714.
[58]
R Development Core Team (2005) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, ISBN 3-900051-07-0, Available: http://www.R-project.org.