Genomic analysis of hybrid rice varieties reveals numerous superior alleles that contribute to heterosis

Nature Communications

Volumn 6, Issue , 2015, Pages

  Huang, Xuehui ^a   Yang, Shihua ^b   Gong, Junyi ^b   Zhao, Yan ^a   Feng, Qi ^a   Gong, Hao ^a   Li, Wenjun ^a   Zhan, Qilin ^a   Cheng, Benyi ^b   Xia, Junhui ^b   Chen, Neng ^b   Hao, Zhongna ^c   Liu, Kunyan ^a   Zhu, Chuanrang ^a   Huang, Tao ^a   Zhao, Qiang ^a   Zhang, Lei ^a   Fan, Danlin ^a   Zhou, Congcong ^a   Lu, Yiqi ^a   Weng, Qijun ^a   Wang, Zi Xuan ^a   Li, Jiayang ^d   Han, Bin ^a   more..

^a FUDAN UNIVERSITY   (China)

^b INSTITUTE OF PLANT PROTECTION   (China)

^c INSTITUTE OF PLANT PROTECTION AND MICROBIOLOGY   (China)

^d INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AGRICULTURAL PRACTICE; ALLELE; DOMINANCE; GENETIC ANALYSIS; GENOMICS; GENOTYPE; GEOACCUMULATION; HIGH YIELDING VARIETY; HYBRID; RICE;

AGRONOMIC TRAIT; ALLELE; ARTICLE; CHROMOSOME 6; CONTROLLED STUDY; CROSS BREEDING; GENE LOCUS; GENETIC ASSOCIATION; GENETIC IMPROVEMENT; GENETIC VARIABILITY; GENOME; GENOMICS; GENOTYPE; GENOTYPE ENVIRONMENT INTERACTION; GRAIN YIELD; HETEROSIS; HETEROZYGOSITY; HYBRID; INBRED STRAIN; MAGNAPORTHE GRISEA; NONHUMAN; PHENOTYPIC VARIATION; PLANT GENETICS; PLANT HEIGHT; PLANT LEAF; RICE; SEQUENCE ALIGNMENT; SINGLE NUCLEOTIDE POLYMORPHISM; XANTHOMONAS ORYZAE; AGRICULTURE; GENETICS; GENOME-WIDE ASSOCIATION STUDY; HETEROZYGOTE; HYBRIDIZATION; ORYZA; PHENOTYPE; PLANT GENOME; QUANTITATIVE TRAIT;

AGRICULTURE; ALLELES; GENE-ENVIRONMENT INTERACTION; GENOME, PLANT; GENOME-WIDE ASSOCIATION STUDY; HETEROZYGOTE; HYBRID VIGOR; HYBRIDIZATION, GENETIC; ORYZA; PHENOTYPE; QUANTITATIVE TRAIT, HERITABLE;

EID: 84923166725     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms7258     Document Type: Article

References (60)

1. Darwin, C. R. The Effects of Cross- and Self-Fertilization in the Vegetable Kingdom (John Murray, 1876).
2. Shull, G. H. The composition of a field of maize. Am. Breed. Assoc. Rep. 4, 296-301 (1908).
3. East, E. M. Inbreeding in Corn (Connecticut Agricultural Experiment Station Report, 1908).
4. Cheng, S. H., Zhuang, J. Y., Fan, Y. Y., Du, J. H. & Cao, L. Y. Progress in research and development on hybrid rice: a super-domesticate in China. Ann. Bot. (London) 100, 959-966 (2007).
5. Li, S., Yang, D. & Zhu, Y. Characterization and use of male sterility in hybrid rice breeding. J. Integr. Plant Biol. 49, 791-804 (2007).
6. Luo, D. et al. A detrimental mitochondrial-nuclear interaction causes cytoplasmic male sterility in rice. Nat. Genet. 45, 573-577 (2013).
7. Bruce, A. B. The Mendelian theory of heredity and the augmentation of vigor. Science 32, 627-628 (1910).
8. Jones, D. F. Dominance of linked factors as a means of accounting for heterosis. Genetics 2, 466-479 (1917).
9. Shull, G. H. The genotypes of maize. Am. Nat. 45, 234-252 (1911).
10. East, E. M. Heterosis. Genetics 21, 375-397 (1936).
11. Minvielle, F. Dominance is not necessary for heterosis: a two-locus model. Genet. Res. 49, 245-247 (1987).
12. Schnell, F. W. & Cockerham, C. C. Multiplicative vs. arbitrary gene action in heterosis. Genetics 131, 461-469 (1992).
13. Moore, S. & Lukens, L. An evaluation of Arabidopsis thaliana hybrid traits and their genetic control. G3 (Bethesda) 1, 571-579 (2011).
14. Krieger, U., Lippman, Z. B. & Zamir, D. The flowering gene SINGLE FLOWER TRUSS drives heterosis for yield in tomato. Nat. Genet. 42, 459-463 (2010).
15. Hollick, J. B. & Chandler, V. L. Epigenetic allelic states of a maize transcriptional regulatory locus exhibit overdominant gene action. Genetics 150, 891-897 (1998).
16. Xiao, J., Li, J., Yuan, L. & Tanksley, S. D. Dominance is the major genetic basis of heterosis in rice as revealed by QTL analysis using molecular markers. Genetics 140, 745-754 (1995).
17. Hua, J. P. et al. Genetic dissection of an elite rice hybrid revealed that heterozygotes are not always advantageous for performance. Genetics 162, 1885-1895 (2002).
18. Zhou, G. et al. Genetic composition of yield heterosis in an elite rice hybrid. Proc. Natl Acad. Sci. USA 109, 15847-15852 (2012).
19. Riedelsheimer, C. et al. Genomic and metabolic prediction of complex heterotic traits in hybrid maize. Nat. Genet. 44, 217-220 (2012).
20. Browning, B. L. & Browning, S. R. A unified approach to genotype imputation and haplotype phase inference for large data sets of trios and unrelated individuals. Am. J. Hum. Genet. 84, 210-223 (2009).
21. Yang, J. et al. A killer-protector system regulates both hybrid sterility and segregation distortion in rice. Science 337, 1336-1340 (2012).
22. Suresh, P. B. et al. Fine mapping of Rf3 and Rf4 fertility restorer loci of WA-CMS of rice (Oryza sativa L.) and validation of the developed marker system for identification of restorer lines. Euphytica 187, 421-435 (2012).
23. Tang, H. et al. The rice restorer Rf4 for wild-abortive cytoplasmic male sterility encodes a mitochondrial-localized PPR protein that functions in reduction of WA352 transcripts. Mol. Plant 7, 1497-1500 (2014).
24. Huang, X. et al. Genome-wide association studies of 14 agronomic traits in rice landraces. Nat. Genet. 42, 961-967 (2010).
25. Huang, X. et al. Genome-wide association study of flowering time and grain yield traits in a worldwide collection of rice germplasm. Nat. Genet. 44, 32-39 (2012).
26. Huang, X. et al. A map of rice genome variation reveals the origin of cultivated rice. Nature 490, 497-501 (2012).
27. Kang, H. M. et al. Variance component model to account for sample structure in genome-wide association studies. Nat. Genet. 42, 348-354 (2010).
28. Wang, Z. Y. et al. The amylose content in rice endosperm is related to the post-transcriptional regulation of the waxy gene. Plant J. 7, 613-622 (1995).
29. Gao, Z. et al. Map-based cloning of the ALK gene, which controls the gelatinization temperature of rice. Sci. China C. Life Sci. 46, 661-668 (2003).
30. Shomura, A. et al. Deletion in a gene associated with grain size increased yields during rice domestication. Nat. Genet. 40, 1023-1028 (2008).
31. Wang, Z. X. et al. The Pib gene for rice blast resistance belongs to the nucleotide binding and leucine-rich repeat class of plant disease resistance genes. Plant J. 19, 55-64 (1999).
32. Liu, G., Lu, G., Zeng, L. & Wang, G. L. Two broad-spectrum blast resistance genes, Pi9(t) and Pi2(t), are physically linked on rice chromosome 6. Mol. Genet. Genomics 267, 472-480 (2002).
33. Berruyer, R. et al. Identification and fine mapping of Pi33, the rice resistance gene corresponding to the Magnaporthe grisea avirulence gene ACE1. Theor. Appl. Genet. 107, 1139-1147 (2003).
34. Ashikari, M. et al. Cytokinin oxidase regulates rice grain production. Science 309, 741-745 (2005).
35. Xue, W. et al. Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice. Nat. Genet. 40, 761-767 (2008).
36. Jiao, Y. et al. Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice. Nat. Genet. 42, 541-544 (2010).
37. Miura, K. et al. OsSPL14 promotes panicle branching and higher grain productivity in rice. Nat. Genet. 42, 545-549 (2010).
38. Fujita, D. et al. NAL1 allele from a rice landrace greatly increases yield in modern indica cultivars. Proc. Natl Acad. Sci. USA 110, 20431-20436 (2014).
39. Kojima, S. et al. Hd3a, a rice ortholog of the Arabidopsis FT gene, promotes transition to flowering downstream of Hd1 under short-day conditions. Plant Cell Physiol. 43, 1096-1105 (2002).
40. Yano, M. et al. 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 (2000).
41. Doi, K. et al. Ehd1, a B-type response regulator in rice, confers short-day promotion of flowering and controls FT-like gene expression independently of Hd1. Gene Dev. 18, 926-936 (2004).
42. Saitoh, K., Onishi, K., Mikami, I., Thidar, K. & Sano, Y. Allelic diversification at the C (OsC1) locus of wild and cultivated rice: nucleotide changes associated with phenotypes. Genetics 168, 997-1007 (2004).
43. Tadege, M. et al. Reciprocal control of flowering time by OsSOC1 in transgenic Arabidopsis and by FLC in transgenic rice. Plant Biotechnol. 1, 361-369 (2003).
44. Yan, W. H. et al. A major QTL, Ghd8, plays pleiotropic roles in regulating grain productivity, plant height, and heading date in rice. Mol. Plant 4, 319-330 (2011).
45. Fan, C. et al. GS3, a major QTL for grain length and weight and minor QTL for grain width and thickness in rice, encodes a putative transmembrane protein. Theor. Appl. Genet. 112, 1164-1171 (2006).
46. Song, X. J., Huang, W., Shi, M., Zhu, M. Z. & Lin, H. X. A QTL for rice grain width and weight encodes a previously unknown RING-type E3 ubiquitin ligase. Nat. Genet. 39, 623-630 (2007).
47. Xu, S., Zhu, D. & Zhang, Q. Predicting hybrid performance in rice using genomic best linear unbiased prediction. Proc. Natl Acad. Sci. USA 111, 12456-12461 (2014).
48. Xu, X. et al. Resequencing 50 accessions of cultivated and wild rice yields markers for identifying agronomically important genes. Nat. Biotechnol. 30, 105-111 (2012).
49. The 3,000 Rice Genomes Project. The 3,000 Rice Genomes Project. GigaScience 3, 7 (2014).
50. Gao, Z.-Y. et al. Dissecting yield-associated loci in super hybrid rice by resequencing recombinant inbred lines and improving parental genome sequences. Proc. Natl Acad. Sci. USA 110, 14492-14497 (2013).
51. Kozarewa, I. et al. Amplification-free Illumina sequencing-library preparation facilitates improved mapping and assembly of (G+C)-biased genomes. Nat. Methods 6, 291-295 (2009).
52. International Rice Genome Sequencing Project. The map-based sequence of the rice genome. Nature 436, 793-800 (2005).
53. Alexander, D. H., Novembre, J. & Lange, K. Fast model-based estimation of ancestry in unrelated individuals. Genome Res. 19, 1655-1664 (2009).
54. Felsenstein, J. PHYLIP: phylogeny inference package (version 3.2). Cladistics. 5, 164-166 (1989).
55. Tamura, K. et al. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731-2739 (2011).
56. Price, A. L. et al. Principal components analysis corrects for stratification in genome-wide association studies. Nat. Genet. 38, 904-909 (2006).
57. Juliano, B. Rice Chemistry and Technology 443-513 (American Association of Cereal Chemists, 1985).
58. Little, R. R., Hilder, G. B. & Dawson, E. H. Differential effect of dilute alkali on 25 varieties of milled white rice. Cereal Chem. 35, 111-126 (1958).
59. Chen, H. et al. Comparative analyses of genomic locations and race specificities of loci for quantitative resistance to Pyricularia grisea in rice and barley. Proc. Natl Acad. Sci. USA 100, 2544-2549 (2003).
60. Churchill, G. A. & Doerge, R. W. Empirical threshold values for quantitative trait mapping. Genetics 138, 963-971 (1994).