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Genetic Architecture of Aluminum Tolerance in Rice () Determined through Genome-Wide Association Analysis and QTL Mapping


Aluminum (Al) toxicity is a primary limitation to crop productivity on acid soils, and rice has been demonstrated to be significantly more Al tolerant than other cereal crops. However, the mechanisms of rice Al tolerance are largely unknown, and no genes underlying natural variation have been reported. We screened 383 diverse rice accessions, conducted a genome-wide association (GWA) study, and conducted QTL mapping in two bi-parental populations using three estimates of Al tolerance based on root growth. Subpopulation structure explained 57% of the phenotypic variation, and the mean Al tolerance in Japonica was twice that of Indica. Forty-eight regions associated with Al tolerance were identified by GWA analysis, most of which were subpopulation-specific. Four of these regions co-localized with a priori candidate genes, and two highly significant regions co-localized with previously identified QTLs. Three regions corresponding to induced Al-sensitive rice mutants (ART1, STAR2, Nrat1) were identified through bi-parental QTL mapping or GWA to be involved in natural variation for Al tolerance. Haplotype analysis around the Nrat1 gene identified susceptible and tolerant haplotypes explaining 40% of the Al tolerance variation within the aus subpopulation, and sequence analysis of Nrat1 identified a trio of non-synonymous mutations predictive of Al sensitivity in our diversity panel. GWA analysis discovered more phenotype–genotype associations and provided higher resolution, but QTL mapping identified critical rare and/or subpopulation-specific alleles not detected by GWA analysis. Mapping using Indica/Japonica populations identified QTLs associated with transgressive variation where alleles from a susceptible aus or indica parent enhanced Al tolerance in a tolerant Japonica background. This work supports the hypothesis that selectively introgressing alleles across subpopulations is an efficient approach for trait enhancement in plant breeding programs and demonstrates the fundamental importance of subpopulation in interpreting and manipulating the genetics of complex traits in rice.


Vyšlo v časopise: Genetic Architecture of Aluminum Tolerance in Rice () Determined through Genome-Wide Association Analysis and QTL Mapping. PLoS Genet 7(8): e32767. doi:10.1371/journal.pgen.1002221
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002221

Souhrn

Aluminum (Al) toxicity is a primary limitation to crop productivity on acid soils, and rice has been demonstrated to be significantly more Al tolerant than other cereal crops. However, the mechanisms of rice Al tolerance are largely unknown, and no genes underlying natural variation have been reported. We screened 383 diverse rice accessions, conducted a genome-wide association (GWA) study, and conducted QTL mapping in two bi-parental populations using three estimates of Al tolerance based on root growth. Subpopulation structure explained 57% of the phenotypic variation, and the mean Al tolerance in Japonica was twice that of Indica. Forty-eight regions associated with Al tolerance were identified by GWA analysis, most of which were subpopulation-specific. Four of these regions co-localized with a priori candidate genes, and two highly significant regions co-localized with previously identified QTLs. Three regions corresponding to induced Al-sensitive rice mutants (ART1, STAR2, Nrat1) were identified through bi-parental QTL mapping or GWA to be involved in natural variation for Al tolerance. Haplotype analysis around the Nrat1 gene identified susceptible and tolerant haplotypes explaining 40% of the Al tolerance variation within the aus subpopulation, and sequence analysis of Nrat1 identified a trio of non-synonymous mutations predictive of Al sensitivity in our diversity panel. GWA analysis discovered more phenotype–genotype associations and provided higher resolution, but QTL mapping identified critical rare and/or subpopulation-specific alleles not detected by GWA analysis. Mapping using Indica/Japonica populations identified QTLs associated with transgressive variation where alleles from a susceptible aus or indica parent enhanced Al tolerance in a tolerant Japonica background. This work supports the hypothesis that selectively introgressing alleles across subpopulations is an efficient approach for trait enhancement in plant breeding programs and demonstrates the fundamental importance of subpopulation in interpreting and manipulating the genetics of complex traits in rice.


Zdroje

1. von UexküllHRMutertE 1995 Global extent, development and economic impact of acid soils. DateRAGrundonNJRaymetGEProbertME Plant-Soil Interactions at Low pH: Principles and Management Dordrecht, Netherlands Kluwer Academic Publishers 5 19

2. KochianLVPinerosMAHoekengaOA 2005 The physiology, genetics and molecular biology of plant aluminum tolerance and toxicity. Plant and Soil 274 175 195

3. FoyC 1988 Plant adaptation to acid, aluminum-toxic soils. Communications in Soil Science and Plant Analysis 19 959 987

4. SasakiTRyanPDelhaizeEHebbDOgiharaY 2006 Sequence upstream of the wheat (Triticum aestivum L.) ALMT1 gene and its relationship to aluminum resistance. Plant and Cell Physiology 47 1343

5. PinerosMShaffJManslankHCarvalho AlvesVKochianL 2005 Aluminum resistance in maize cannot be solely explained by root organic acid exudation. A comparative physiological study. Plant Physiology 137 231

6. FurukawaJYamajiNWangHMitaniNMurataY 2007 An aluminum-activated citrate transporter in barley. Plant and Cell Physiology 48 1081

7. CaniatoFGuimaraesCSchaffertRAlvesVKochianL 2007 Genetic diversity for aluminum tolerance in sorghum. Theoretical and Applied Genetics 114 863 876

8. FamosoAClarkRShaffJCraftEMcCouchS 2010 Development of a novel Aluminum tolerance phenotyping platform used for comparisons of cereal Aluminum tolerance and investigations into rice Aluminum tolerance mechanisms. Plant Physiology 153 1678

9. SasakiTYamamotoYEzakiBKatsuharaMAhnS 2004 A wheat gene encoding an aluminum-activated malate transporter. The Plant Journal 37 645 653

10. MagalhaesJGarvinDWangYSorrellsMKleinP 2004 Comparative mapping of a major aluminum tolerance gene in sorghum and other species in the Poaceae. Genetics 167 1905 1914

11. MinellaESorrellsM 1992 Aluminum tolerance in barley: genetic relationships among genotypes of diverse origin. Crop Science 32 593 598

12. Ninamango-CardenasFTeixeira GuimarãesCMartinsPNetto ParentoniSPortilho CarneiroN 2003 Mapping QTLs for aluminum tolerance in maize. Euphytica 130 223 232

13. NguyenVTBurowMDNguyenHTLeBTLeTD 2001 Molecular mapping of genes conferring aluminum tolerance in rice (Oryza sativa L.). Theoretical and Applied Genetics 102 1002 1010

14. SasakiTYamamotoYEzakiEKatsuharaMRyanPR 2004 A gene encoding an aluminum-activated malate transporter segregates with aluminum tolerance in wheat. Plant Journal 37 645 653

15. MagalhaesJLiuJGuimarãesCLanaUAlvesV 2007 A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in sorghum. Nature Genetics 39 1156 1161

16. HoekengaOVisionTShaffJMonforteALeeG 2003 Identification and characterization of aluminum tolerance loci in Arabidopsis (Landsberg erecta x Columbia) by quantitative trait locus mapping. A physiologically simple but genetically complex trait. Plant Physiology 132 936

17. NguyenVNguyenBSarkarungSMartinezCPatersonA 2002 Mapping of genes controlling aluminum tolerance in rice: comparison of different genetic backgrounds. Molecular Genetics and Genomics 267 772 780

18. HuangXFengQQianQZhaoQWangL 2009 High-throughput genotyping by whole-genome resequencing. Genome Research 19 1068

19. YamajiNHuangCNagaoSYanoMSatoY 2009 A zinc finger transcription factor ART1 regulates multiple genes implicated in aluminum tolerance in rice. The Plant Cell 21 3339 3349

20. XiaJYamajiNKasaiTMaJ 2010 Plasma membrane-localized transporter for aluminum in rice. Proceedings of the National Academy of Sciences 107 18381

21. LarsenPCancelJRoundsMOchoaV 2007 Arabidopsis ALS1 encodes a root tip and stele localized half type ABC transporter required for root growth in an aluminum toxic environment. Planta 225 1447 1458

22. LarsenPGeislerMJonesCWilliamsKCancelJ 2005 ALS3 encodes a phloem localized ABC transporter like protein that is required for aluminum tolerance in Arabidopsis. The Plant Journal 41 353 363

23. MaJFShenRZhaoZWissuwaMTakeuchiY 2002 Response of rice to Al stress and identification of quantitative trait Loci for Al tolerance. Plant Cell Physiology 43 652 659

24. HuangCYamajiNMitaniNYanoMNagamuraY 2009 A bacterial-type ABC transporter is involved in aluminum tolerance in rice. The Plant Cell 21 655 667

25. NguyenBDBrarDSBuiBCNguyenTBPhamLN 2003 Identification and mapping of the QTL for aluminum tolerance introgressed from the new source, Oryza rufipogon Griff., into indica rice (Oryza sativa L.). Theoretical and Applied Genetics 106 583 593

26. MaJShenRZhaoZWissuwaMTakeuchiY 2002 Response of rice to Al stress and identification of quantitative trait loci for Al tolerance. Plant and Cell Physiology 43 652

27. XueYJiangLSuNWangJDengP 2007 The genetic basic and fine-mapping of a stable quantitative-trait loci for aluminium tolerance in rice. Planta 227 255 262

28. XueYWanJJiangLWangCLiuL 2006 Identification of quantitative trait loci associated with aluminum tolerance in rice (Oryza sativa L.). Euphytica 150 37 45

29. WuPLiaoCDHuBYiKKJinWZ 2000 QTLs and epistasis for aluminum tolerance in rice (Oryza sativa L.) at different seedling stages. Theoretical Applied Genetics 100 1295 1303

30. OkaHI 1988 Indica-Japonica differentiation of rice cultivars. OkaHI Origin of Cultivated Rice Tokyo Elsevier Science/Japan Scientific Societies Press 141 179

31. BarbierP 1989 Genetic variation and ecotypic differentiation in the wild rice species O. rufipogon II. Influence of the mating system and life history traits on the genetic structure of populations. Japanese Journal of Genetics 63 273 285

32. MaJBennetzenJL 2004 Rapid recent growth and divergence of rice nuclear genomes. Proceedings of the National Academy of Sciences 101 12404 12410

33. VitteCIshiiTLamyFBrarDPanaudO 2004 Genomic paleontology provides evidence for two distinct origins of Asian rice (Oryza sativa L.). Molecular Genetics and Genomics 272 504 511

34. LondoJChiangYHungKChiangTSchaalB 2006 Phylogeography of Asian wild rice, Oryza rufipogon, reveals multiple independent domestications of cultivated rice, Oryza sativa. Proceedings of the National Academy of Sciences 103 9578

35. KovachMJSweeneyMTMcCouchSR 2007 New insights into the history of rice domestication. Trends in Genetics 23 578 587

36. KovachMMcCouchS 2008 Leveraging natural diversity: back through the bottleneck. Current Opinion in Plant Biology 11 193 200

37. ZhuQGeS 2005 Phylogenetic relationships among A-genome species of the genus Oryza revealed by intron sequences of four nuclear genes. New Phytologist 167 249 265

38. ZhouHXieZGeS 2003 Microsatellite analysis of genetic diversity and population genetic structure of a wild rice (Oryza rufipogon Griff.) in China. Theoretical and Applied Genetics 107 332 339

39. SweeneyMThomsonMChoY-GParkY-JWilliamsonS 2007 Global dissemination of a single mutation conferring white pericarp in rice. PLoS Genet 3 e133 doi:10.1371/journal.pgen.0030133

40. GarrisAJTaiTHCoburnJRKresovichSMcCouchS 2005 Genetic structure and diversity in Oryza sativa L. Genetics 169 1631 1638

41. CaicedoALWilliamsonSHHernandezRDBoykoAFledel-AlonA 2007 Genome-wide patterns of nucleotide polymorphism in domesticated rice. PLoS Genet 3 e163 doi:10.1371/journal.pgen.0030163

42. ZhaoKWrightMKimballJEizengaGMcClungA 2010 Genomic diversity and introgression in O. sativa reveal the impact of domestication and breeding on the rice genome. PLoS ONE 5 e10780 doi:10.1371/journal.pone.0010780

43. KhushG 1997 Origin, dispersal, cultivation and variation of rice. Plant Molecular Biology 35 25 34

44. GlaszmannJC 1987 Isozymes and classification of Asian rice varieties. Theoretical and Applied Genetics 74 21 30

45. GarrisAJMcCouchSRKresovichS 2003 Population structure and its effect on haplotype diversity and linkage disequilibrium surrounding the xa5 locus of rice (Oryza sativa L.). Genetics 165 759 769

46. OlsenKCaicedoAPolatoNMcClungAMcCouchS 2006 Selection under domestication: evidence for a sweep in the rice Waxy genomic region. Genetics 173 975

47. MatherKCaicedoAPolatoNOlsenKMcCouchS 2007 The extent of linkage disequilibrium in rice (Oryza sativa L.). Genetics 177 2223

48. RakshitSRakshitAMatsumuraHTakahashiYHasegawaY 2007 Large-scale DNA polymorphism study of Oryza sativa and O. rufipogon reveals the origin and divergence of Asian rice. Theoretical and Applied Genetics 114 731 743

49. McNallyKLChildsKLBohnertRDavidsonRMZhaoK 2009 Genomewide SNP variation reveals relationships among landraces and modern varieties of rice. Proceedings of the National Academy of Sciences 106 12273 12278

50. ReichDCargillMBolkSIrelandJSabetiP 2001 Linkage disequilibrium in the human genome. Nature 411 199 204

51. DalyMRiouxJSchaffnerSHudsonTLanderE 2001 High-resolution haplotype structure in the human genome. Nature Genetics 29 229 232

52. JeffreysAKauppiLNeumannR 2001 Intensely punctate meiotic recombination in the class II region of the major histocompatibility complex. Nature Genetics 29 217 222

53. KimSPlagnolVHuTTToomajianCClarkRM 2007 Recombination and linkage disequilibrium in Arabidopsis thaliana. Nature Genetics 39 1151 1155

54. NordborgMBorevitzJOBergelsonJBerryCCChoryJ 2002 The extent of linkage disequilibrium in Arabidopsis thaliana. Nature Genetics 30 190 193

55. JungMChingABhattramakkiDDolanMTingeyS 2004 Linkage disequilibrium and sequence diversity in a 500-kbp region around the adh1 locus in elite maize germplasm. Theoretical and Applied Genetics 109 681 689

56. YuJBucklerES 2006 Genetic association mapping and genome organization of maize. Current Opinion in Biotechnology 17 155 160

57. ChingACaldwellKJungMDolanMSmithO 2002 SNP frequency, haplotype structure and linkage disequilibrium in elite maize inbred lines. BMC Genetics 3 19

58. TenaillonMSawkinsMLongAGautRDoebleyJ 2001 Patterns of DNA sequence polymorphism along chromosome 1 of maize (Zea mays ssp. mays L.). Proceedings of the National Academy of Sciences of the United States of America 98 9161

59. RemingtonDThornsberryJMatsuokaYWilsonLWhittS 2001 Structure of linkage disequilibrium and phenotypic associations in the maize genome. Proceedings of the National Academy of Sciences of the United States of America 98 11479

60. PlattAHortonMHuangYLiYAnastasioA 2010 The scale of population structure in Arabidopsis thaliana. PLoS Genet 6 e1000843 doi:10.1371/journal.pgen.1000843

61. AtwellSHuangYSVilhjalmssonBJWillemsGHortonM 2010 Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines. Nature 465 627 631

62. ZhaoKAranzanaMKimSListerCShindoC 2007 An Arabidopsis example of association mapping in structured samples. PLoS Genet 3 e4 doi:10.1371/journal.pgen.0030004

63. YuJPressoirGBriggsWBiIYamasakiM 2005 A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nature Genetics 38 203 208

64. HuangXWeiXSangTZhaoQFengQ 2010 Genome-wide association studies of 14 agronomic traits in rice landraces. Nature Genetics 42 926 927

65. ZhaoKTCWEizengaGCWrightMHAliMLPriceAHNortonGJIslamMRReynoldsAMezeyJMcClungAMBustamanteCDMcCouchSR 2011 Genome-wide association mapping reveals rich genetic architecture of complex traits in Oryza sativa. Nature Communications (Accepted)

66. AliMMcClungAMJiaMHKimballJAMcCouchSREizengaGC 2011 Rice Diversity Panel “evaluated for genetic and agro-morphological diversity between subpopulations and its geographic distribution”. Crop Science (Accepted March 18, 2011)

67. TungC-WZhaoKWrightMAliMJungJ 2010 Development of a research platform for dissecting phenotype–genotype associations in rice (Oryza spp.). Rice 1 13

68. McCouchSRZhaoKWrightMTungC-WEbanaK 2010 Development of genome-wide SNP assays for rice. Breeding Science 60 524 535

69. AhmadiNDubreuil-TranchantCCourtoisBFoncekaDThisD IRRI, editor New resources and integrated maps for IR64 × Azucena: a reference population in rice. 2005 19–23 November 2005 Manila, Philippines International Rice Research Institute

70. LinSYSasakiTYanoM 1998 Mapping quantitative trait loci controlling seed dormancy and heading date in rice, Oryza sativa L., using backcross inbred lines. Theoretical and Applied Genetics 96 997 1003

71. KangHZaitlenNWadeCKirbyAHeckermanD 2008 Efficient control of population structure in model organism association mapping. Genetics 178 1709

72. LiYHuangYBergelsonJNordborgMBorevitzJO 2010 Association mapping of local climate-sensitive quantitative trait loci in Arabidopsis thaliana. Proceedings of the National Academy of Sciences 107 21199 21204

73. MaronLGKirstMMaoCMilnerMJMenossiM 2008 Transcriptional profiling of aluminum toxicity and tolerance responses in maize roots. New Phytologist 179 116 128

74. KrillAKirstMKochianLBucklerEHoekengaO 2010 Association and linkage analysis of Aluminum tolerance genes in maize. PLoS ONE 5 e9958 doi:10.1371/journal.pone.0009958

75. SangTGeS 2007 The puzzle of rice domestication. Journal of Integrative Plant Biology 49 760 768

76. HanBXueY 2003 Genome-wide intraspecific DNA-sequence variations in rice. Current Opinion in Plant Biology 6 134 138

77. LiuXLinFWangLPanQ 2007 The in silico map-based cloning of Pi36, a rice coiled-coil–nucleotide-binding site–leucine-rich repeat gene that confers race-specific resistance to the blast fungus. Genetics 176 2541 2549

78. KumagaiMWangLUedaS 2010 Genetic diversity and evolutionary relationships in genus Oryza revealed by using highly variable regions of chloroplast DNA. Gene 462 44 51

79. BeavisWD 1994 The power and deceit of QTL experiments: lessons from comparative QTL studies. 250 265 Proceedings of the 49th Annual Corn and Sorghum Research Conference, American Seed Trade Association, Washington, DC

80. BaierACSomersDJGusiafsonJP 1995 Aluminium tolerance in wheat: correlating hydroponic evaluations with field and soil performances. Plant Breeding 114 291 296

81. BastenCWeirBZengZ 2002 QTL Cartographer, version 1.16. Department of Statistics, North Carolina State University, Raleigh, NC

82. PriceAPattersonNPlengeRWeinblattMShadickN 2006 Principal components analysis corrects for stratification in genome-wide association studies. Nature Genetics 38 904 909

83. BarrettJCFryBMallerJDalyMJ 2005 Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21 263 265

84. PritchardJStephensMDonnellyP 2000 Inference of population structure using multilocus genotype data. Genetics 155 945

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