Mapping regulatory variants controlling gene expression in drought response and tolerance in maize.

Shengxue Liu, Cuiping Li, Hongwei Wang, Shuhui Wang, Shiping Yang, Xiaohu Liu, Jianbing Yan, Bailin Li, Mary Beatty, Gina Zastrow-Hayes, Shuhui Song, Feng Qin
Author Information
  1. Shengxue Liu: State Key Laboratory of Plant Physiology and Biochemistry, College of Biological Sciences, China Agricultural University, Beijing, 100193, China.
  2. Cuiping Li: National Genomics Data Center & CAS Key Laboratory of Genome Sciences and Information, Beijing Institute of Genomics, Chinese Academy of Sciences, and China National Center for Bioinformation, Beijing, 100101, China.
  3. Hongwei Wang: Agricultural College, Yangtze University, Jingzhou, 434025, China.
  4. Shuhui Wang: State Key Laboratory of Plant Physiology and Biochemistry, College of Biological Sciences, China Agricultural University, Beijing, 100193, China.
  5. Shiping Yang: State Key Laboratory of Plant Physiology and Biochemistry, College of Biological Sciences, China Agricultural University, Beijing, 100193, China.
  6. Xiaohu Liu: State Key Laboratory of Plant Physiology and Biochemistry, College of Biological Sciences, China Agricultural University, Beijing, 100193, China.
  7. Jianbing Yan: National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan, 430070, China.
  8. Bailin Li: Corteva Agriscience, Johnston, IA, 50131, USA.
  9. Mary Beatty: Corteva Agriscience, Johnston, IA, 50131, USA.
  10. Gina Zastrow-Hayes: Corteva Agriscience, Johnston, IA, 50131, USA.
  11. Shuhui Song: National Genomics Data Center & CAS Key Laboratory of Genome Sciences and Information, Beijing Institute of Genomics, Chinese Academy of Sciences, and China National Center for Bioinformation, Beijing, 100101, China. songshh@big.ac.cn.
  12. Feng Qin: State Key Laboratory of Plant Physiology and Biochemistry, College of Biological Sciences, China Agricultural University, Beijing, 100193, China. qinfeng@cau.edu.cn. ORCID

Abstract

BACKGROUND: Gene expression is a key determinant of cellular response. Natural variation in gene expression bridges genetic variation to phenotypic alteration. Identification of the regulatory variants controlling the gene expression in response to drought, a major environmental threat of crop production worldwide, is of great value for drought-tolerant gene identification.
RESULTS: A total of 627 RNA-seq analyses are performed for 224 maize accessions which represent a wide genetic diversity under three water regimes; 73,573 eQTLs are detected for about 30,000 expressing genes with high-density genome-wide single nucleotide polymorphisms, reflecting a comprehensive and dynamic genetic architecture of gene expression in response to drought. The regulatory variants controlling the gene expression constitutively or drought-dynamically are unraveled. Focusing on dynamic regulatory variants resolved to genes encoding transcription factors, a drought-responsive network reflecting a hierarchy of transcription factors and their target genes is built. Moreover, 97 genes are prioritized to associate with drought tolerance due to their expression variations through the Mendelian randomization analysis. One of the candidate genes, Abscisic acid 8'-hydroxylase, is verified to play a negative role in plant drought tolerance.
CONCLUSIONS: This study unravels the effects of genetic variants on gene expression dynamics in drought response which allows us to better understand the role of distal and proximal genetic effects on gene expression and phenotypic plasticity. The prioritized drought-associated genes may serve as direct targets for functional investigation or allelic mining.

Keywords

References

  1. Bioinformatics. 2014 Apr 1;30(7):923-30 [PMID: 24227677]
  2. Plant Physiol. 2009 Feb;149(2):825-34 [PMID: 19036833]
  3. Annu Rev Plant Biol. 2006;57:781-803 [PMID: 16669782]
  4. Bioinformatics. 2007 Oct 1;23(19):2633-5 [PMID: 17586829]
  5. Bioinformatics. 2005 Jan 15;21(2):263-5 [PMID: 15297300]
  6. Plant Physiol. 2011 Oct;157(2):692-705 [PMID: 21844310]
  7. Genetics. 2014 Jun;197(2):573-89 [PMID: 24700103]
  8. Nat Genet. 2011 Sep 25;43(11):1160-3 [PMID: 21946354]
  9. Nature. 2014 Jan 9;505(7482):208-11 [PMID: 24270809]
  10. Nat Genet. 2016 May;48(5):481-7 [PMID: 27019110]
  11. Nat Protoc. 2016 Sep;11(9):1650-67 [PMID: 27560171]
  12. Nat Genet. 2016 Mar;48(3):245-52 [PMID: 26854917]
  13. Proc Natl Acad Sci U S A. 2015 Nov 3;112(44):E6010-9 [PMID: 26483487]
  14. Plant J. 2015 Sep;83(6):1046-58 [PMID: 26234706]
  15. Plant Cell. 2019 Mar;31(3):602-626 [PMID: 30755461]
  16. Cell. 2016 Oct 6;167(2):313-324 [PMID: 27716505]
  17. Nat Genet. 2018 Sep;50(9):1289-1295 [PMID: 30061735]
  18. Nat Genet. 2019 Jun;51(6):1052-1059 [PMID: 31152161]
  19. Nat Genet. 2013 Jan;45(1):43-50 [PMID: 23242369]
  20. Nature. 2017 Jun 22;546(7659):524-527 [PMID: 28605751]
  21. Plant Cell. 2010 Apr;22(4):1313-32 [PMID: 20418496]
  22. Genome Biol. 2020 Jul 6;21(1):163 [PMID: 32631406]
  23. BMC Plant Biol. 2014 Dec 10;14:344 [PMID: 25492673]
  24. Plant Cell. 1995 Feb;7(2):195-201 [PMID: 7756830]
  25. Plant Physiol. 2017 Oct;175(2):708-720 [PMID: 28830938]
  26. J Exp Bot. 2018 Oct 12;69(21):5177-5189 [PMID: 30137393]
  27. Genome Res. 2010 Sep;20(9):1297-303 [PMID: 20644199]
  28. Proc Natl Acad Sci U S A. 2007 Jan 30;104(5):1708-13 [PMID: 17237218]
  29. Mol Plant. 2017 Mar 6;10(3):414-426 [PMID: 27381443]
  30. Plant Cell. 2014 Sep;26(9):3472-87 [PMID: 25248552]
  31. Proc Natl Acad Sci U S A. 2007 Jul 3;104(27):11376-81 [PMID: 17595297]
  32. Nat Commun. 2019 Jun 14;10(1):2632 [PMID: 31201335]
  33. Nat Genet. 2019 Apr;51(4):611-617 [PMID: 30926969]
  34. Curr Opin Biotechnol. 2006 Apr;17(2):155-60 [PMID: 16504497]
  35. Science. 2019 Aug 16;365(6454):658-664 [PMID: 31416957]
  36. Planta. 2019 Feb;249(2):351-362 [PMID: 30206696]
  37. Mol Plant. 2019 Mar 4;12(3):447-460 [PMID: 30802553]
  38. J Exp Bot. 2010 Jun;61(6):1655-69 [PMID: 20194926]
  39. Nat Biotechnol. 2015 Mar;33(3):290-5 [PMID: 25690850]
  40. Nature. 2017 Oct 11;550(7675):204-213 [PMID: 29022597]
  41. Nat Genet. 2012 Jun 03;44(7):803-7 [PMID: 22660545]
  42. Proc Natl Acad Sci U S A. 2013 Oct 15;110(42):16969-74 [PMID: 24089449]
  43. Plant Physiol. 2005 Jun;138(2):1117-25 [PMID: 15908602]
  44. FEBS Lett. 2007 Jul 24;581(18):3356-62 [PMID: 17604024]
  45. Plant Cell Environ. 2015 Jan;38(1):35-49 [PMID: 24738645]
  46. Nucleic Acids Res. 2019 Jan 8;47(D1):D8-D14 [PMID: 30365034]
  47. Essays Biochem. 2015;58:29-48 [PMID: 26374885]
  48. Genomics Proteomics Bioinformatics. 2017 Feb;15(1):14-18 [PMID: 28387199]
  49. Bioinformatics. 2010 Jan 1;26(1):139-40 [PMID: 19910308]
  50. Nat Protoc. 2012 Feb 16;7(3):500-7 [PMID: 22343431]
  51. Science. 2010 Feb 12;327(5967):812-8 [PMID: 20110467]
  52. Nat Genet. 2016 Oct;48(10):1233-41 [PMID: 27526320]
  53. Science. 2014 May 2;344(6183):516-9 [PMID: 24786079]
  54. Plant Cell. 2001 Nov;13(11):2393-407 [PMID: 11701877]
  55. Nat Methods. 2015 Apr;12(4):357-60 [PMID: 25751142]
  56. Nat Commun. 2015 Sep 21;6:8326 [PMID: 26387805]
  57. BMC Plant Biol. 2014 Nov 29;14:327 [PMID: 25432517]
  58. Theor Appl Genet. 2019 Mar;132(3):817-849 [PMID: 30798332]
  59. Nat Genet. 2010 Apr;42(4):355-60 [PMID: 20208535]
  60. Bioinformatics. 2009 Aug 15;25(16):2078-9 [PMID: 19505943]
  61. Nat Commun. 2014 Oct 08;5:5087 [PMID: 25295980]
  62. Nat Rev Genet. 2015 Apr;16(4):197-212 [PMID: 25707927]
  63. Plant Cell. 2009 Feb;21(2):622-41 [PMID: 19234086]
  64. Plant Cell. 2009 Jan;21(1):54-71 [PMID: 19155348]
  65. Science. 2016 Nov 4;354(6312): [PMID: 27811239]
  66. Nucleic Acids Res. 2018 Jan 4;46(D1):D944-D949 [PMID: 29069473]
  67. Nat Commun. 2014 Mar 17;5:3438 [PMID: 24633423]

MeSH Term

Abscisic Acid
Droughts
Gene Expression Regulation, Plant
Genome-Wide Association Study
Mendelian Randomization Analysis
Osmoregulation
Quantitative Trait Loci
Regulatory Elements, Transcriptional
Transcription Factors
Water
Zea mays

Chemicals

Transcription Factors
Water
Abscisic Acid