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PMID: 22701078 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Genic and nongenic contributions to natural variation of quantitative traits in maize.

Genome research ·Vol. 22 ·No. 12 ·2012-12-00 ·Pages 2436-44

Li X, Zhu C, Yeh CT, Wu W, Takacs EM, Petsch KA, Tian F, Bai G, Buckler ES, Muehlbauer GJ, Timmermans MC, Scanlon MJ, Schnable PS, Yu J

Abstract

The complex genomes of many economically important crops present tremendous challenges to understand the genetic control of many quantitative traits with great importance in crop production, adaptation, and evolution. Advances in genomic technology need to be integrated with strategic genetic design and novel perspectives to break new ground. Complementary to individual-gene-targeted research, which remains challenging, a global assessment of the genomic distribution of trait-associated SNPs (TASs) discovered from genome scans of quantitative traits can provide insights into the genetic architecture and contribute to the design of future studies. Here we report the first systematic tabulation of the relative contribution of different genomic regions to quantitative trait variation in maize. We found that TASs were enriched in the nongenic regions, particularly within a 5-kb window upstream of genes, which highlights the importance of polymorphisms regulating gene expression in shaping the natural variation. Consistent with these findings, TASs collectively explained 44%-59% of the total phenotypic variation across maize quantitative traits, and on average, 79% of the explained variation could be attributed to TASs located in genes or within 5 kb upstream of genes, which together comprise only 13% of the genome. Our findings suggest that efficient, cost-effective genome-wide association studies (GWAS) in species with complex genomes can focus on genic and promoter regions.

MeSH Terms
Chromosome Mapping Genes, Plant Genetic Variation Linkage Disequilibrium Mutation Phenotype Polymorphism, Single Nucleotide Quantitative Trait Loci RNA, Plant/genetics Sequence Analysis, RNA Transcription Initiation Site Transcriptome Zea mays/genetics
Chemicals
RNA, Plant
Authors & Affiliations
14 authors, click to expand affiliations / ORCID
Li Xianran
Department of Agronomy, Kansas State University, Manhattan, Kansas 66506, USA.
Zhu Chengsong
Yeh Cheng-Ting
Wu Wei
Takacs Elizabeth M
Petsch Katherine A
Tian Feng
Bai Guihua
Buckler Edward S
Muehlbauer Gary J
Timmermans Marja C P
Scanlon Michael J
Schnable Patrick S
Yu Jianming
References (53)
53 references, click to expand
  1. Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines.
    Nature. 2010 Jun 3;465(7298):627-31 PMID: 20336072
  2. Allele-specific up-regulation of FGFR2 increases susceptibility to breast cancer.
    PLoS Biol. 2008 May 6;6(5):e108 PMID: 18462018
  3. Interactions of liguleless1 and liguleless2 function during ligule induction in maize.
    Genetics. 1996 Dec;144(4):1871-82 PMID: 8978070
  4. Towards a complete resolution of the genetic architecture of disease.
    Trends Genet. 2010 Oct;26(10):438-42 PMID: 20813421
  5. A characterization of the MADS-box gene family in maize.
    Plant J. 1995 Dec;8(6):845-54 PMID: 8580958
  6. Activation of CRABS CLAW in the Nectaries and Carpels of Arabidopsis.
    Plant Cell. 2005 Jan;17(1):25-36 PMID: 15598802
  7. Genomic and metabolic prediction of complex heterotic traits in hybrid maize.
    Nat Genet. 2012 Jan 15;44(2):217-20 PMID: 22246502
  8. The maize gene liguleless2 encodes a basic leucine zipper protein involved in the establishment of the leaf blade-sheath boundary.
    Genes Dev. 1998 Jan 15;12(2):208-18 PMID: 9490265
  9. Selection for translation efficiency on synonymous polymorphisms in recent human evolution.
    Genome Biol Evol. 2011;3:749-61 PMID: 21803767
  10. The genetic architecture of maize flowering time.
    Science. 2009 Aug 7;325(5941):714-8 PMID: 19661422
  11. Genetic properties of the maize nested association mapping population.
    Science. 2009 Aug 7;325(5941):737-40 PMID: 19661427
  12. Pervasive gene content variation and copy number variation in maize and its undomesticated progenitor.
    Genome Res. 2010 Dec;20(12):1689-99 PMID: 21036921
  13. Rare variants create synthetic genome-wide associations.
    PLoS Biol. 2010 Jan 26;8(1):e1000294 PMID: 20126254
  14. The molecular genetics of crop domestication.
    Cell. 2006 Dec 29;127(7):1309-21 PMID: 17190597
  15. The regulatory regions required for B' paramutation and expression are located far upstream of the maize b1 transcribed sequences.
    Genetics. 2002 Oct;162(2):917-30 PMID: 12399399
  16. Genome-wide atlas of transcription during maize development.
    Plant J. 2011 May;66(4):553-63 PMID: 21299659
  17. Genome-wide patterns of genetic variation among elite maize inbred lines.
    Nat Genet. 2010 Nov;42(11):1027-30 PMID: 20972441
  18. The B73 maize genome: complexity, diversity, and dynamics.
    Science. 2009 Nov 20;326(5956):1112-5 PMID: 19965430
  19. A first-generation haplotype map of maize.
    Science. 2009 Nov 20;326(5956):1115-7 PMID: 19965431
  20. Ectopic expression of the knox homeo box gene rough sheath1 alters cell fate in the maize leaf.
    Genes Dev. 1995 Sep 15;9(18):2292-304 PMID: 7557382
  21. Two small regulatory RNAs establish opposing fates of a developmental axis.
    Genes Dev. 2007 Apr 1;21(7):750-5 PMID: 17403777
  22. Leafbladeless1 is required for dorsoventrality of lateral organs in maize.
    Development. 1998 Aug;125(15):2813-23 PMID: 9655804
  23. Potential etiologic and functional implications of genome-wide association loci for human diseases and traits.
    Proc Natl Acad Sci U S A. 2009 Jun 9;106(23):9362-7 PMID: 19474294
  24. Genome-wide association study of leaf architecture in the maize nested association mapping population.
    Nat Genet. 2011 Feb;43(2):159-62 PMID: 21217756
  25. Genome-wide association studies of 14 agronomic traits in rice landraces.
    Nat Genet. 2010 Nov;42(11):961-7 PMID: 20972439
  26. Conserved noncoding genomic sequences associated with a flowering-time quantitative trait locus in maize.
    Proc Natl Acad Sci U S A. 2007 Jul 3;104(27):11376-81 PMID: 17595297
  27. fw2.2: a quantitative trait locus key to the evolution of tomato fruit size.
    Science. 2000 Jul 7;289(5476):85-8 PMID: 10884229
  28. A fast and flexible statistical model for large-scale population genotype data: applications to inferring missing genotypes and haplotypic phase.
    Am J Hum Genet. 2006 Apr;78(4):629-44 PMID: 16532393
  29. SNP discovery via 454 transcriptome sequencing.
    Plant J. 2007 Sep;51(5):910-8 PMID: 17662031
  30. Screening the human exome: a comparison of whole genome and whole transcriptome sequencing.
    Genome Biol. 2010;11(5):R57 PMID: 20598109
  31. Stem cell transcriptome profiling via massive-scale mRNA sequencing.
    Nat Methods. 2008 Jul;5(7):613-9 PMID: 18516046
  32. Differentiation of the maize subgenomes by genome dominance and both ancient and ongoing gene loss.
    Proc Natl Acad Sci U S A. 2011 Mar 8;108(10):4069-74 PMID: 21368132
  33. ANALYZING TABLES OF STATISTICAL TESTS.
    Evolution. 1989 Jan;43(1):223-225 PMID: 28568501
  34. Genome partitioning of genetic variation for complex traits using common SNPs.
    Nat Genet. 2011 Jun;43(6):519-25 PMID: 21552263
  35. Cytokinin oxidase regulates rice grain production.
    Science. 2005 Jul 29;309(5735):741-5 PMID: 15976269
  36. Genetic design and statistical power of nested association mapping in maize.
    Genetics. 2008 Jan;178(1):539-51 PMID: 18202393
  37. Fine mapping association study and functional analysis implicate a SNP in MSMB at 10q11 as a causal variant for prostate cancer risk.
    Hum Mol Genet. 2009 Apr 1;18(7):1368-75 PMID: 19153072
  38. Fast and SNP-tolerant detection of complex variants and splicing in short reads.
    Bioinformatics. 2010 Apr 1;26(7):873-81 PMID: 20147302
  39. Biological, clinical and population relevance of 95 loci for blood lipids.
    Nature. 2010 Aug 5;466(7307):707-13 PMID: 20686565
  40. Gene discovery and annotation using LCM-454 transcriptome sequencing.
    Genome Res. 2007 Jan;17(1):69-73 PMID: 17095711
  41. The Human Gene Mutation Database: 2008 update.
    Genome Med. 2009 Jan 22;1(1):13 PMID: 19348700
  42. Variation explained in mixed-model association mapping.
    Heredity (Edinb). 2010 Oct;105(4):333-40 PMID: 20145669
  43. Statistical significance for genomewide studies.
    Proc Natl Acad Sci U S A. 2003 Aug 5;100(16):9440-5 PMID: 12883005
  44. The developmental dynamics of the maize leaf transcriptome.
    Nat Genet. 2010 Dec;42(12):1060-7 PMID: 21037569
  45. Mixed linear model approach adapted for genome-wide association studies.
    Nat Genet. 2010 Apr;42(4):355-60 PMID: 20208535
  46. Synonymous but not the same: the causes and consequences of codon bias.
    Nat Rev Genet. 2011 Jan;12(1):32-42 PMID: 21102527
  47. Uncovering the roles of rare variants in common disease through whole-genome sequencing.
    Nat Rev Genet. 2010 Jun;11(6):415-25 PMID: 20479773
  48. The role of QTLs in the breeding of high-yielding rice.
    Trends Plant Sci. 2011 Jun;16(6):319-26 PMID: 21429786
  49. A distant upstream enhancer at the maize domestication gene tb1 has pleiotropic effects on plant and inflorescent architecture.
    Nat Genet. 2006 May;38(5):594-7 PMID: 16642024
  50. Finding the missing heritability of complex diseases.
    Nature. 2009 Oct 8;461(7265):747-53 PMID: 19812666
  51. Genes identified by visible mutant phenotypes show increased bias toward one of two subgenomes of maize.
    PLoS One. 2011 Mar 10;6(3):e17855 PMID: 21423772
  52. A unified mixed-model method for association mapping that accounts for multiple levels of relatedness.
    Nat Genet. 2006 Feb;38(2):203-8 PMID: 16380716
  53. What has natural variation taught us about plant development, physiology, and adaptation?
    Plant Cell. 2009 Jul;21(7):1877-96 PMID: 19574434
Article Info
Journal
Genome research
Abbr.
Genome Res
ISSN
1549-5469
Published
2012-12-00
Epub
2012-00-14
Pages
2436-44
Language
English
Region
United States
NLM ID
9518021
PMCID
PMC3514673
Subset
IM
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