Genome-Wide Association Studies Reveal the Genetic Basis of Ionomic Variation in Rice.

Meng Yang, Kai Lu, Fang-Jie Zhao, Weibo Xie, Priya Ramakrishna, Guangyuan Wang, Qingqing Du, Limin Liang, Cuiju Sun, Hu Zhao, Zhanyi Zhang, Zonghao Liu, Jingjing Tian, Xin-Yuan Huang, Wensheng Wang, Huaxia Dong, Jintao Hu, Luchang Ming, Yongzhong Xing, Gongwei Wang, Jinhua Xiao, David E Salt, Xingming Lian
Author Information
  1. Meng Yang: National Key Laboratory of Crop Genetic Improvement and National Center of Plant Gene Research (Wuhan), Huazhong Agricultural University, Wuhan 430070, China.
  2. Kai Lu: National Key Laboratory of Crop Genetic Improvement and National Center of Plant Gene Research (Wuhan), Huazhong Agricultural University, Wuhan 430070, China.
  3. Fang-Jie Zhao: State Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing 210095, China.
  4. Weibo Xie: National Key Laboratory of Crop Genetic Improvement and National Center of Plant Gene Research (Wuhan), Huazhong Agricultural University, Wuhan 430070, China.
  5. Priya Ramakrishna: Centre for Plant Integrative Biology, School of Biosciences, University of Nottingham, Sutton Bonington Campus, Loughborough LE12 5RD, United Kingdom.
  6. Guangyuan Wang: National Key Laboratory of Crop Genetic Improvement and National Center of Plant Gene Research (Wuhan), Huazhong Agricultural University, Wuhan 430070, China.
  7. Qingqing Du: National Key Laboratory of Crop Genetic Improvement and National Center of Plant Gene Research (Wuhan), Huazhong Agricultural University, Wuhan 430070, China.
  8. Limin Liang: National Key Laboratory of Crop Genetic Improvement and National Center of Plant Gene Research (Wuhan), Huazhong Agricultural University, Wuhan 430070, China.
  9. Cuiju Sun: National Key Laboratory of Crop Genetic Improvement and National Center of Plant Gene Research (Wuhan), Huazhong Agricultural University, Wuhan 430070, China.
  10. Hu Zhao: National Key Laboratory of Crop Genetic Improvement and National Center of Plant Gene Research (Wuhan), Huazhong Agricultural University, Wuhan 430070, China.
  11. Zhanyi Zhang: National Key Laboratory of Crop Genetic Improvement and National Center of Plant Gene Research (Wuhan), Huazhong Agricultural University, Wuhan 430070, China.
  12. Zonghao Liu: National Key Laboratory of Crop Genetic Improvement and National Center of Plant Gene Research (Wuhan), Huazhong Agricultural University, Wuhan 430070, China.
  13. Jingjing Tian: National Key Laboratory of Crop Genetic Improvement and National Center of Plant Gene Research (Wuhan), Huazhong Agricultural University, Wuhan 430070, China.
  14. Xin-Yuan Huang: State Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing 210095, China.
  15. Wensheng Wang: National Key Laboratory of Crop Genetic Improvement and National Center of Plant Gene Research (Wuhan), Huazhong Agricultural University, Wuhan 430070, China.
  16. Huaxia Dong: National Key Laboratory of Crop Genetic Improvement and National Center of Plant Gene Research (Wuhan), Huazhong Agricultural University, Wuhan 430070, China.
  17. Jintao Hu: National Key Laboratory of Crop Genetic Improvement and National Center of Plant Gene Research (Wuhan), Huazhong Agricultural University, Wuhan 430070, China.
  18. Luchang Ming: National Key Laboratory of Crop Genetic Improvement and National Center of Plant Gene Research (Wuhan), Huazhong Agricultural University, Wuhan 430070, China.
  19. Yongzhong Xing: National Key Laboratory of Crop Genetic Improvement and National Center of Plant Gene Research (Wuhan), Huazhong Agricultural University, Wuhan 430070, China.
  20. Gongwei Wang: National Key Laboratory of Crop Genetic Improvement and National Center of Plant Gene Research (Wuhan), Huazhong Agricultural University, Wuhan 430070, China.
  21. Jinhua Xiao: National Key Laboratory of Crop Genetic Improvement and National Center of Plant Gene Research (Wuhan), Huazhong Agricultural University, Wuhan 430070, China.
  22. David E Salt: Centre for Plant Integrative Biology, School of Biosciences, University of Nottingham, Sutton Bonington Campus, Loughborough LE12 5RD, United Kingdom.
  23. Xingming Lian: National Key Laboratory of Crop Genetic Improvement and National Center of Plant Gene Research (Wuhan), Huazhong Agricultural University, Wuhan 430070, China xmlian@mail.hzau.edu.cn.

Abstract

Rice () is an important dietary source of both essential micronutrients and toxic trace elements for humans. The genetic basis underlying the variations in the mineral composition, the ionome, in rice remains largely unknown. Here, we describe a comprehensive study of the genetic architecture of the variation in the rice ionome performed using genome-wide association studies (GWAS) of the concentrations of 17 mineral elements in rice grain from a diverse panel of 529 accessions, each genotyped at ∼6.4 million single nucleotide polymorphism loci. We identified 72 loci associated with natural ionomic variations, 32 that are common across locations and 40 that are common within a single location. We identified candidate genes for 42 loci and provide evidence for the causal nature of three genes, the sodium transporter gene for sodium, for molybdenum, and , , for nitrogen. Comparison of GWAS data from rice versus Arabidopsis () also identified well-known as well as new candidates with potential for further characterization. Our study provides crucial insights into the genetic basis of ionomic variations in rice and serves as an important foundation for further studies on the genetic and molecular mechanisms controlling the rice ionome.

References

  1. Annu Rev Plant Biol. 2010;61:535-59 [PMID: 20192735]
  2. Sci Rep. 2017 Dec 18;7(1):17704 [PMID: 29255144]
  3. PLoS Biol. 2014 Dec 02;12(12):e1002009 [PMID: 25464340]
  4. PLoS Genet. 2012;8(8):e1002839 [PMID: 22876191]
  5. Plant J. 2003 Aug;35(3):418-27 [PMID: 12887592]
  6. Plant J. 2011 Jun;66(5):852-62 [PMID: 21457363]
  7. Nat Genet. 2008 Jun;40(6):761-7 [PMID: 18454147]
  8. Plant J. 2015 Jan;81(1):13-23 [PMID: 25267402]
  9. BMC Plant Biol. 2013 Feb 27;13:32 [PMID: 23445750]
  10. Mol Plant. 2015 Jun;8(6):946-57 [PMID: 25747843]
  11. Mol Plant. 2016 Jun 6;9(6):787-97 [PMID: 27212388]
  12. Curr Opin Plant Biol. 2009 Jun;12(3):247-9 [PMID: 19524481]
  13. Plant Physiol. 2010 Aug;153(4):1747-58 [PMID: 20566706]
  14. Theor Appl Genet. 2014 Jan;127(1):137-65 [PMID: 24231918]
  15. PLoS Genet. 2012 Sep;8(9):e1002923 [PMID: 22969436]
  16. PLoS One. 2012;7(7):e39865 [PMID: 22808069]
  17. Nat Commun. 2016 Jul 08;7:12138 [PMID: 27387148]
  18. Proc Natl Acad Sci U S A. 2010 Sep 21;107(38):16500-5 [PMID: 20823253]
  19. PLoS One. 2013 Dec 10;8(12):e82569 [PMID: 24340041]
  20. G3 (Bethesda). 2016 Dec 7;6(12):4175-4183 [PMID: 27770027]
  21. Plant Cell Rep. 2005 Jan;23(8):540-7 [PMID: 15309499]
  22. Science. 1995 Sep 22;269(5231):1714-8 [PMID: 17821643]
  23. J Exp Bot. 2014 Sep;65(17):4849-61 [PMID: 24963001]
  24. Plant Cell. 2012 May;24(5):2155-67 [PMID: 22589467]
  25. Plant Biotechnol J. 2013 Jan;11(1):87-100 [PMID: 23116435]
  26. J Integr Plant Biol. 2009 Jan;51(1):84-92 [PMID: 19166498]
  27. Annu Rev Plant Biol. 2008;59:709-33 [PMID: 18251712]
  28. Bioinformatics. 2007 Oct 1;23(19):2633-5 [PMID: 17586829]
  29. Curr Opin Plant Biol. 2013 Jun;16(3):328-34 [PMID: 23587938]
  30. New Phytol. 2015 Dec;208(4):1056-66 [PMID: 26147403]
  31. Plant Physiol. 2014 Feb;164(2):735-47 [PMID: 24390391]
  32. Nat Genet. 2010 Nov;42(11):961-7 [PMID: 20972439]
  33. Rice (N Y). 2016 Dec;9(1):49 [PMID: 27671163]
  34. Nat Commun. 2016 Oct 04;7:12767 [PMID: 27698483]
  35. J Exp Bot. 2016 Jun;67(12):3645-53 [PMID: 26931170]
  36. Sci Rep. 2016 Jan 25;6:19792 [PMID: 26806528]
  37. Plant J. 1994 Aug;6(2):271-82 [PMID: 7920717]
  38. Nucleic Acids Res. 2015 Jan;43(Database issue):D1018-22 [PMID: 25274737]
  39. Nat Genet. 2012 Jun 17;44(7):825-30 [PMID: 22706313]
  40. Mol Plant. 2011 Mar;4(2):319-30 [PMID: 21148627]
  41. Hum Genet. 2012 May;131(5):747-56 [PMID: 22143225]
  42. Nat Genet. 2014 Jun;46(6):652-6 [PMID: 24777451]
  43. Environ Geochem Health. 2013 Apr;35(2):161-70 [PMID: 22760687]
  44. Theor Appl Genet. 2003 Dec;108(1):131-40 [PMID: 13679990]
  45. Rice (N Y). 2017 Dec;10(1):9 [PMID: 28353179]
  46. Nat Biotechnol. 2003 Oct;21(10):1215-21 [PMID: 12949535]
  47. J Agric Food Chem. 2015 Sep 16;63(36):8008-16 [PMID: 26317332]
  48. PLoS Genet. 2015 Nov 23;11(11):e1005648 [PMID: 26599497]
  49. PLoS Genet. 2010 Nov 11;6(11):e1001193 [PMID: 21085628]
  50. Nucleic Acids Res. 2006 Jan 1;34(Database issue):D745-8 [PMID: 16381972]
  51. PLoS One. 2014 Feb 25;9(2):e89685 [PMID: 24586963]
  52. Proc Natl Acad Sci U S A. 2015 Sep 29;112(39):E5411-9 [PMID: 26358652]
  53. Trends Plant Sci. 2006 Dec;11(12):610-7 [PMID: 17092760]
  54. PLoS One. 2012;7(4):e35121 [PMID: 22558123]
  55. J Exp Bot. 2007;58(9):2369-87 [PMID: 17556767]
  56. Annu Rev Plant Biol. 2016 Apr 29;67:489-512 [PMID: 27128467]
  57. Nature. 2018 Aug;560(7720):595-600 [PMID: 30111841]
  58. Proc Natl Acad Sci U S A. 2009 Jul 28;106(30):12273-8 [PMID: 19597147]
  59. Plant Cell. 2012 Dec;24(12):4793-805 [PMID: 23277364]
  60. Nat Genet. 2015 Jul;47(7):834-8 [PMID: 26053497]
  61. New Phytol. 2011 Jan;189(1):190-9 [PMID: 20840506]
  62. Trends Plant Sci. 2009 Dec;14(12):660-8 [PMID: 19783197]
  63. Nat Genet. 2016 Aug;48(8):927-34 [PMID: 27322545]
  64. Sci Total Environ. 2002 Jan 23;282-283:9-24 [PMID: 11852908]
  65. J Genet. 2008 Dec;87(3):305-10 [PMID: 19147920]
  66. New Phytol. 2009;182(1):49-84 [PMID: 19192191]
  67. Cold Spring Harb Protoc. 2009 Oct;2009(10):pdb.ip71 [PMID: 20147036]
  68. Proc Natl Acad Sci U S A. 2007 Nov 20;104(47):18807-12 [PMID: 18003916]
  69. Nature. 2012 Oct 25;490(7421):497-501 [PMID: 23034647]
  70. Springerplus. 2016 Dec 9;5(1):2086 [PMID: 28018794]
  71. PLoS Genet. 2011 Aug;7(8):e1002221 [PMID: 21829395]
  72. Methods. 2001 Dec;25(4):402-8 [PMID: 11846609]
  73. Nat Biotechnol. 2012 Mar 11;30(4):360-4 [PMID: 22407351]
  74. Nat Genet. 2014 Jul;46(7):714-21 [PMID: 24908251]
  75. Nat Genet. 2005 Oct;37(10):1141-6 [PMID: 16155566]
  76. Trends Plant Sci. 2009 Oct;14(10):563-73 [PMID: 19716745]
  77. Plant Physiol. 2012 Feb;158(2):590-600 [PMID: 22198273]
  78. New Phytol. 2012 Feb;193(3):650-64 [PMID: 22142234]
  79. Plant Cell. 2009 Oct;21(10):3326-38 [PMID: 19861554]
  80. Theor Appl Genet. 2011 Jan;122(1):49-61 [PMID: 20717799]
  81. Trends Plant Sci. 2002 Jul;7(7):309-15 [PMID: 12119168]
  82. Nat Genet. 2011 Dec 04;44(1):32-9 [PMID: 22138690]
  83. PLoS Genet. 2008 Feb 29;4(2):e1000004 [PMID: 18454190]
  84. Annu Rev Plant Biol. 2014;65:531-51 [PMID: 24274033]
  85. Nature. 2005 Aug 11;436(7052):793-800 [PMID: 16100779]
  86. Nat Genet. 2016 Apr;48(4):447-56 [PMID: 26950093]

MeSH Term

Genetic Variation
Genome-Wide Association Study
Genotype
Linkage Disequilibrium
Oryza
Polymorphism, Single Nucleotide
Quantitative Trait Loci

Word Cloud

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