Sub-genomic selection patterns as a signature of breeding in the allopolyploid Brassica napus genome

BMC Genomics

Volumn 15, Issue 1, 2014, Pages

  Qian, Lunwen ^a   Qian, Wei ^b   Snowdon, Rod J ^a  

^a JUSTUS LIEBIG UNIVERSITY   (Germany)

^b SOUTHWEST UNIVERSITY   (China)

Author keywords

Haplotype; LD; Population genomics; Rapeseed; Selection

Indexed keywords

ERUCIC ACID; GLUCOSINOLATE; GENETIC MARKER;

AGRONOMIC TRAIT; ALLOPOLYPLOIDY; ARTICLE; BREEDING LINE; GENE LINKAGE DISEQUILIBRIUM; GENE POOL; GENETIC ASSOCIATION; GENETIC CONSERVATION; GENETIC RECOMBINATION; GENETIC SELECTION; GENETIC VARIABILITY; GENOTYPE; HAPLOTYPE; INTROGRESSION; NONHUMAN; PLANT BREEDING; PLANT SEED; POPULATION STRUCTURE; PRINCIPAL COORDINATE ANALYSIS; QUANTITATIVE TRAIT LOCUS; RAPESEED; SEED QUALITY; SEQUENCE ANALYSIS; SINGLE NUCLEOTIDE POLYMORPHISM; BREEDING; GENETIC MARKER; GENETICS; GENOMICS; GROWTH, DEVELOPMENT AND AGING; PHYLOGENY; PLANT GENOME; POLYPLOIDY; SEASON;

BRASSICA NAPUS; BREEDING; GENETIC MARKERS; GENOME, PLANT; GENOMICS; HAPLOTYPES; LINKAGE DISEQUILIBRIUM; PHYLOGENY; POLYMORPHISM, SINGLE NUCLEOTIDE; POLYPLOIDY; QUANTITATIVE TRAIT LOCI; SEASONS; SEEDS;

EID: 84964313711     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-15-1170     Document Type: Article

References (69)

1. Uzunova M, Ecke W, Weißleder K, Röbbelen G: Mapping the genome of rapeseed (Brassica napus L.). I. Construction of an RFLP linkage map and localization of QTLs for seed glucosinolate content. Theor Appl Genet 1935, 90:194-204.
2. Flint-Garcia SA, Thornsberry JM, Buckler ES: Structure of linkage disequilibrium in plants. Annu Rev Plant Biol 2003, 54:357-374.
3. Ersoz ES, Yu J, Buckler ES: Applications of linkage disequilibrium and association mapping in crop plants. Dordrecht: Genomics-assisted crop improvement Springer; 2007:97-120.
4. Li H, Peng ZY, Yang XH, Wang WD, Fu JJ, Wang JH, Han YJ, Chai YC, Guo TT, Yang N, Liu J, Warburton ML, Cheng YB, Hao XM, Zhang P, Zhao JY, Liu YJ GY, Li JS, Yan JB: Genome-wide association study dissects the genetic architecture of oil biosynthesis in maize kernels. Nat Genetics 2013, 45:43-U72.
5. Zhao K, Tung CW, Eizenga GC, Wright MH, Ali ML, Price AH, Norton GJ, Islam MR, Reynolds A, Mezey J, McClung AM, Bustamante CD, McCouch SR: Genome-wide association mapping reveals a rich genetic architecture of complex traits in Oryza sativa. Nat Commun 2011, 2:246.
6. Bhosale SU, Stich B, Rattunde HF, Weltzien E, Haussmann BI, Hash CT, Ramu P, Cuevas HE, Paterson AH, Melchinger AE, Parzies HK: Association analysis of photoperiodic flowering time genes in west and central African sorghum [Sorghum bicolor (L.) Moench]. BMC Plant Biol 2012, 12:32.
7. Edwards D, Batley J, Snowdon RJ: Accessing complex crop genomes with next-generation sequencing. Theor Appl Genet 2013, 126:1-11.
8. Marchini J, Cardon LR, Phillips MS, Donnelly P: The eVects of human population structure on large genetic association studies. Nat Genetics 2004, 36:512-517.
9. Bus A, Korber N, Snowdon RJ, Stich B: Patterns of molecular variation in a species-wide germplasm set of Brassica napus. Theor Appl Genet 2011, 123:1413-1423.
10. Xiao Y, Cai D, Yang W, Ye W, Younas M, Wu J, Liu K: Genetic structure and linkage disequilibrium pattern of a rapeseed (Brassica napus L.) association mapping association mapping in crop plants. Dordrecht: Genomics-assisted crop improvement Springer; 2012:97-120.
11. Hamblin MT, Salas Fernandez MG, Casa AM, Mitchell SE, Paterson AH, Kresovich S: Equilibrium processes cannot explain high levels of short-and medium-range linkage disequilibrium in the domesticated grass Sorghum bicolor. Genetics 2005, 171:1247-1256.
12. Bouchet S, Pot D, Deu M, Rami JF, Billot C, Perrier X, Rivallan R, Gardes L, Xia L, Wenzl P, Kilian A, Glaszmann JC: Genetic structure, linkage disequilibrium and signature of selection in Sorghum: lessons from physically anchored DArT markers. PLoS One 2012, 7:e33470.
13. Bekele WA, Wieckhorst S, Friedt W, Snowdon RJ: High-throughput genomics in sorghum: from whole-genome resequencing to a SNP screening array. Plant Biotechnol J 2013, 11:1112-1125.
14. Remington DL, Thornsberry JM, Matsuoka Y, Wilson LM, Whitt SR, Doebley J, Kresovich S, Goodman MM, Buckler ES: Structure of linkage disequilibrium and phenotypic associations in the maize genome. Proc Natl Acad Sci U S A 2001, 98:11479-11484.
15. Ching A, Caldwell KS, Jung M, Dolan M, Smith OS, Tingey S, Morgante M, Rafalski AJ: SNP frequency, haplotype structure and linkage disequilibrium in elite maize inbred lines. BMC Genet 2002, 3:19.
16. Palaisa KA, Morgante M, Williams M, Rafalski A: Contrasting effects of selection on sequence diversity and linkage disequilibrium at two phytoene synthase loci. Plant Cell 2003, 15:1795-1806.
17. Yan JB, Shah T, Warburton ML, Buckler ES, McMullen MD, Crouch J: Genetic characterization and linkage disequilibrium estimation of a global maize collection using SNP markers. PLoS One 2009, 4:e8451.
18. Jin L, Lu Y, Xiao P, Sun M, Corke H, Bao J: Genetic diversity and population structure of a diverse set of rice germplasm for association mapping. Theor Appl Genet 2010, 121:475-487.
19. Mather KA, Caicedo AL, Polato NR, Olsen KM, McCouch S, Purugganan MD: The extent of linkage disequilibrium in rice (Oryza sativa L.). Genetics 2007, 177:2223-2232.
20. Nordborg M, Hu TT, Ishino Y, Jhaveri J, Toomajian C, Zheng H, Bakker E, Calabrese P, Gladstone J, Goyal R, Jakobsson M, Kim S, Morozov Y, Padhukasahasram B, Plagnol V, Rosenberg NA, Shah C, Wall JD, Wang J, Zhao K, Kalbfleisch T, Schulz V, Kreitman M, Bergelson J: The pattern of polymorphism in Arabidopsis thaliana. PLoS Biol 2005, 3:e196.
21. Hagenblad J, Nordborg M: Sequence variation and haplotype structure surrounding the flowering time locus FRI in Arabidopsis thaliana. Genetics 2002, 161:289-298.
22. Ecke W, Clemens R, Honsdorf N, Becker HC: Extent and structure of linkage disequilibrium in canola quality winter rapeseed (Brassica napus L.). Theor Appl Genet 2010, 120:921-931.
23. Zou J, Jiang C, Cao Z, Li R, Long Y, Chen S, Meng J: Association mapping of seed oil content in Brassica napus and comparison with quantitative trait loci identified from linkage mapping. Genome 2010, 53:908-916.
24. Cruciani F, Santolamazza P, Shen PD, Macaulay V, Moral P, Olckers A, Modiano D, Holmes S, Destro-Bisol G, Coia V, Wallace DC, Oefner PJ, Torroni A, Cavalli-Sforza LL, Scozzari R, Underhill PA: A back migration from Asia to sub-Saharan Africa is supported by high-resolution analysis of human Y-chromosome haplotypes. Am J Hum Genet 2002, 70:1197-1214.
25. Gore MA, Chia JM, Elshire RJ, Sun Q, Ersoz ES, Hurwitz BL, Peiffer JA, McMullen MD, Grills GS, Ross-Ibarra J, Ware DH, Buckler ES: A first-generation haplotype map of maize. Science 2009, 326:1115-1117.
26. Delourme R, Falentin C, Fomeju BF, Boillot M, Lassalle G, Andre I, Duarte J, Gauthier V, Lucante N, Marty A, Pauchon M, Pichon JP, Ribiere N, Trotoux G, Blanchard P, Riviere N, Martinant JP, Pauquet J: High-density SNP-based genetic map development and linkage disequilibrium assessment in Brassica napus L. BMC Genomics 2013, 14:120.
27. Allender CJ, King GJ: Origins of the amphiploid species Brassica napus L. investigated by chloroplast and nuclear molecular markers. BMC Plant Biol 2010, 10:54.
28. Hasan M, Seyis F, Badani AG, Pons-Kuhnemann J, Lühs W, Friedt W, Snowdon RJ: Surveying genetic diversity in the Brassica napus gene pool using SSR markers. Genet Res Crop Evol 2006, 53:793-802.
29. Murray MG, Thompsom WF: Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 1980, 8:4321-4325.
30. Chalhoub B, Denoeud F, Liu S, Parkin IAP, Tang H, Wang X, Chiquet J, Belcram H, Tong C, Samans B, Corréa M, Da Silva C, Just J, Falentin C, Koh CS, Le Clainche I, Bernard M, Bento P, Noel B, Labadie K, Alberti A, Charles M, Arnaud D, Guo H, Daviaud C, Alamery S, Jabbari K, Zhao M, Edger PP, Chelaifa H et al.: Early allopolyploid evolution in the post-neolithic Brassica napus oilseed genome. Science 2014. in press.
31. Nei M: Genetic distance between populations. Am Nat 1972, 106:283-292.
32. Liu KJ, Muse SV: PowerMarker: an integrated analysis environment for genetic marker analysis. Bioinformatics 2005, 21:2128-2129.
33. Pritchard JK, Stephens M, Donnelly P: Inference of population structure using multilocus genotype data. Genetics 2000, 155:945-959.
34. Rohlf FJ: NTSYS-pc. Numerical Taxonomy and Multivariate Analysis System, Version 2.1. New York: Exeter Software; 2000.
35. Rambaut A: Fig Tree version 1.3.1. [computer program]. 2009 [http://tree.bio. ed.ac.uk].
36. Hardy OJ, Vekemans X: spagedi: a versatile computer program to analyze spatial genetic structure at the individual or population levels. Mol Ecol Notes 2002, 2:618-620.
37. Yu JM, Pressoir G, Briggs WH, Bi IV, Yamasaki M, Doebley JF, McMullen MD, Gaut BS, Nielsen DM, Holland JB, Kresovich S, Buckler ES: A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet 2006, 38:203-208.
38. Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES: TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 2007, 23:2633-2635.
39. Barrett JC, Fry B, Maller J, Daly MJ: Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 2005, 21:263-265.
40. Gabriel SB, Schaffner SF, Nguyen H, Moore JM, Roy J, Blumenstiel B, Higgins J, DeFelice M, Lochner A, Faggart M, Liu-Cordero SN, Rotimi C, Adeyemo A, Cooper R, Ward R, Lander ES, Daly MJ, Altshuler D: The structure of haplotype blocks in the human genome. Science 2002, 296:2225-2229.
41. Hall TA: BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT Nucleic Acids Symposium Series, Volume 41.; 1999:95-98.
42. Soderlund C, Bomhoff M, Nelson W: SyMAP: A turnkey synteny system with application to multiple large duplicated plant sequenced genomes. Nucleic Acids Res 2011, 10:e68.
43. Shin J-H, Blay S, McNeney B, Graham J: LDheatmap: an R function for graphical display of pairwise linkage disequilibria between single nucleotide polymorphisms. J Stat Soft 2006, 16:1-10.
44. Roscoe TJ, Lessire R, Puyaubert J, Renard M, Delseny M: Mutations in the fatty acid elongation 1 gene are associated with a loss of beta-ketoacyl-CoA synthase activity in low erucic acid rapeseed. FEBS Lett 2001, 492:107-111.
45. Chen S, Nelson MN, Ghamkhar K, Fu T, Cowling WA: Divergent patterns of allelic diversity from similar origins: thecase of oilseed rape (Brassica napus L.) in China and Australia. Genome 2008, 51:1-10.
46. Qian W, Meng J, Li M, Frauen M, Sass O, Noack J, Jung C: Introgression of genomic components from Chinese Brassica rapa contributes to widening the genetic diversity in rapeseed (B. napus L.), with emphasis on the evolution of Chinese rapeseed. Theor Appl Genet 2006, 113:49-54.
47. Liu H: Rapeseed genetics and breeding. Shanghai: Shanhai Science and Technology Press; 1985:559-566.
48. Shiga T: Rapa breeding by interspecific crossing between Brassica napus and Brassica campestris in japan. Jpn Agric Res Quart 1970, 5:5-10.
49. Wall JD, Pritchard JK: Assessing the performance of the haplotype block model of linkage disequilibrium. Am J Hum Genet 2003, 73:502-515.
50. Buckler E, Gore M: An Arabidopsis haplotype map takes root. Nat Genet 2007, 39:1056-1057.
51. Mace ES, Tai S, Gilding EK, Li Y, Prentils PJ, Bian L, Campbell BC, Hu W, Innes DJ, Han X, Cruickshank A, Dai C, Frere C, Zhang H, Hunt CH, Wang X, Shatte T, Wang M, Su Z, Li J, Lin X, Godwin ID, Jordan DR, Wang J: Whole-genome sequencing reveals untapped genetic potential in Africa's indigenous cereal crop sorgum. Nat Commun 2013, 4:2320.
52. Leflon M, Grandont L, Eber F, Huteau V, Coriton O, Chelysheva L, Jenczewski E, Chèvre AM: Crossovers get a boost in Brassica allotriploid and allotetraploid hybrids. Plant Cell 2010, 22:2253-2264.
53. Downey RK, Klassen AL, Stringam GR: Rapeseed and Mustard. In Hybridization of crop plants. Edited by Fehr WR, Hadley H. Madison, WI: ASA, CSA; 1980:495-509.
54. Bennett RA, Thiagarajah MR, King JR, Rahman MH: Interspecific cross of Brassica oleracea var. alboglabra and B.napus: effects of growth condition and silique age on the efficiency of hybrid production, and inheritance of erucic acid in the self-pollinated backcross generation. Euphytica 2008, 164:593-601.
55. Gorelick R: Transposable elements suppress recombination in all meiotic eukaryotes, including automictic ancient asexuals: a reply to Schön and Martens. J Nat Hist 2003, 37:903-909.
56. Rafalski A, Morgante M: Corn and humans: recombination and linkage disequilibrium in two genomes of similar size. Trends Genet 2004, 20:103-111.
57. Olsson G: Species crosses within the genus Brassica. Hereditas 1960, 46:351.
58. McNaughton IH: Swedes and Rapes. In Evolution of Crop Plants. Edited by Simmonds NW. London: Longman; 1976:53-56.
59. Guryev V, Smits BMG, van de Belt J, Verheul M, Hubner N, Cuppen E: Haplotype block structure is conserved across mammals. Plos Genetic 2006, 2:1111-1118.
60. Wang N, Li F, Chen B, Xu K, Yan G, Qian J, Li J, Gao G, Bancroft I, Meng J, King GJ, Wu X: Genome-wide investigation of genetic changes during modern breeding of Brassica napus. Theor Appl Genet 2014, 127:1817-1829.
61. Mei J, Li Q, Qian L, Fu Y, Li J, Frauen M, Qian W: Genetic investigation of the origination of allopolyploid with virtually synthesized lines: application to the C subgenome of Brassica napus. Heredity 2011, 106:955-961.
62. Rygulla W, Friedt W, Seyis F, Lühs W, Eynck C, von Tiedemann A, Snowdon RJ: Combination of resistance to Verticillium longisporum from zero erucic acid Brassica oleracea and oilseed Brassica rapa genotypes in resynthesized rapeseed (Brassica napus) lines. Plant Breed 2007, 126:596-602.
63. Rygulla W, Snowdon RJ, Eynck C, von Tiedemann A, Lühs W, Friedt W: Broadening the genetic basis of Verticillium longisporum resistance in Brassica napus by interspecific hybridisation. Phytopathology 2007, 97:1391-1396.
64. Ding Y, Mei J, Li Q, Liu Y, Wan H, Wang L, Becker HC, Qian W: Improvement of Sclerotinia sclerotiorum resistance in Brassica napus by using B. oleracea. Genet Resour Crop Evol 2013, 60:1615-1619.
65. Jesske T, Olberg B, Schierholt A, Becker HC: Resynthesized lines from domesticated and wild Brassica taxa and their hybrids with B. napus L.: genetic diversity and hybrid yield. Theor Appl Genet 2013, 126:1053-1065.
66. Cornille A, Gladieux P, Smulders MJM, Roldan-Ruiz I, Laurens F, Le Cam B, Nersesyan A, Clavel J, Olonova M, Feugey L, Gabrielyan I, Zhang XG, Tenaillon MI, Giraud T: New insight into the history of domesticated apple: secondary contribution of the European wild apple to the genome of cultivated varieties. Plos Genetics 2012, 8:e1002703.
67. Luo MC, Yang ZL, You FM, Kawahara T, Waines JG, Dvorak J: The structure of wild and domesticated emmer wheat populations, gene flow between them, and the site of emmer domestication. Theor Appl Genet 2007, 114:947-959.
68. Myles S, Boyko AR, Owens CL, Brown PJ, Grassi F, Aradhya MK, Prins B, Reynolds A, Chia JM, Ware D, Bustamante CD, Buckler ES: Genetic structure and domestication history of the grape. Proc Natl Acad Sci U S A 2011, 108:3530-3535.
69. Harper AL, Trick M, Higgins J, Fraser F, Clissold L, Wells R, Hattori C, Werner P, Bancroft I: Associative transcriptomics of traits in the polyploid crop species Brassica napus. Nat Biotechnol 2012, 30:798-802.