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Genome-Wide View of Breeding History and Selection in North American Maize
Dr. Jeffrey Ross-Ibarra
University of California at Davis
Patterns of diversity across the genome are reflective of the historical processes of
selection, drift, and mutation that have acted on a species during its evolution. Here, we
apply population genetic analysis of two genomic datasets to assess the spatial and
temporal signatures of evolution in the maize genome. We first describe genome-wide
patterns of evolution during two epochs of selection, domestication and modern breeding,
using full-genome resequencing of a number of maize and teosinte lines. Then, using a
chronologically-stratified panel of corn belt lines, we dissect temporal patterns of ancestry
and selection in greater detail across the 80+ years of North American corn breeding. We
find distinct impacts of selection during domestication and modern breeding on diversity
and gene expression, identify candidate regions targeted by selection, and describe changes
in genetic structure and ancestry during the evolution of modern corn belt lines.
HISTORICAL GENOMICS OF MAIZE
Jeffrey Ross-Ibarra
www.rilab.org
Acknowledgements
Ed Buckler (Cornell, USDA)
Jeff Glaubitz (Cornell)
Major Goodman (NC State)
Mike McMullen (Missouri, USDA)
Chi Song (BGI)
Nathan Springer (Minnesota)
Doreen Ware (CSHL, USDA)
Xun Xu (BGI)
Matthew Hufford Joost van Heerwaarden Tanja Pyhäjärvi Jer-Ming Chia
HISTORICAL GENOMICS OF MAIZE






3
%





3


3
%
02




%
22222222222222222222222222222222222222222222222222222222222222200000000000000000000000000000000222222000022022222022200000000000000000000000000000000000000000000000000000000000000000022222200000000000000000000000020000000
%
2+
Spatial resolution -- genome resequencing
Temporal resolution -- SNP genotyping
HISTORICAL GENOMICS OF MAIZE






3
%





3


3
%




%
2222222222222222222222222222222222222222222222222000000000000000000022022020020222200200000000000000000000000000000000000000222220000000000000000020000000
%
2+
Spatial resolution -- genome resequencing
Temporal resolution -- SNP genotyping
ρ
0.0020.0060.01
00.010.020.030.04
ρρ
ππ
lower 1% cent10
cM/Mb
ρ
Chr 10
Maize Hapmap I: low-copy fraction of genome
Gore et al. 2009 Science
• Re-sequenced low-copy portion of genome of 27 inbreds
• High diversity genome, but large regions of low recombination
• Identified low diversity putative targets of selection
• No comparison to older material
• Cannot distinguish domestication from modern improvement
Chia et al. Submitted
Maize Hapmap II: full genome resequencing
75 resequenced genomes  21M SNPs75 resequenced genomes  21M SNPs
Sequenced
Genomes
Sequence
Depth
Locality
Improved 35 5.04 X
13 Temperate, 13 Tropical,
3 Mixed, 6 Chinese
Landraces 23 5.34 X
9 South American,
14 North American
parviglumis 14 3.81 X
4 Jalisco/Nayarit,
9 Balsas, 1 Oaxaca
1 1Oaxaca
mexicana 2 6.83 X 1 Jalisco, 1 Morelos
Tripsacum 1 12.62 X Colombia
parviglumis
Landraces
Improved Lines
Domestication
Improvement
Hufford et al. Submitted
Maize
Parviglumis
Maize
Parviglumis
Genic Tajima's D
Tajima's D
Density
-4 -2 0 2 4
0.00.10.20.30.40.5
Hufford et al. Submitted
Maize
Parviglumis
Maize
Parviglumis
Genic Tajima's D
Tajima's D
Density
-4 -2 0 2 4
0.00.10.20.30.40.5
Density
0.00.10.20.30.40.5
Genome-wide Tajima's D
Tajima's D
Density
-4 -2 0 2 4
0.00.10.20.30.4
Hufford et al. Submitted
Chen et al. 2010
Genome Research
COG3-like FMP25-like frq PAC10-like SEC14-like NSL1-like NCU02261
B
Carib
LA
Out
Ellison et al. 2011 PNAS
• Cross-Population Composite Likelihood Ratio
• Identifies extended regions of differentiation
• Compares to simulated model
• Define selected regions, estimate s
Artificial selection in the maize genome
• Stronger selection during
domestication (s~0.015 vs. s~0.003)
• Selection strength consistent with
archaeology  natural selection
• Continued selection on domestication
genes (18% overlap)
• ~3,000 genes in selected regions.
Identified ~1100 candidates
• 5-10% of selected regions had no genes
Hufford et al. Submitted
he maize genome
log s
Frequency
-6 -5 -4 -3 -2
050001500025000
domestication
improvement
Gore et al. Science 2009
Mb chr 8
proportion
FST
Mb chr 8
proportion
0.00.20.40.60.81.0
fixed shared unique temperate unique tropicalemfixed shared unique temperate unique tropical
0 20 40 60 80 100 120 140 160 180
00.050.150.250.35
Population-specific selection
Population-specific selection
Hufford et al. Submitted
• Many population-specific loci
• Stronger overall estimate of selection
• Still weaker than domestication
• Lower power to rule out drift
Candidate genes for maize improvement
Hufford et al. Submitted
Selection on the transcriptome
• Expression at 18K genes of 27 maize and teosinte using Nimblegen array
• Domestication directly selected on candidate gene expression
• Breeding has worked with highly expressed genes
• Modern breeding selected for heterosis in expression
Candidates: DOM IMP
Change in
expression
* --
Decreased
variance
* *
Tissue
specificity#
--
overall higher
expression
Dominance in
crosses#
-- inter  intra
# Data from Stupar et al. 2008 BMC Plant Bio; Sekhon et al. 2011 Plant J.
Hufford et al. Submitted
Regions with no genes likely regulatory
teosintemaize
Swanson-Wagner et al. Submitted
Expression
Genetic load in modern maize
• ~1% of SNPs disrupts predicted
protein
• 10,117 premature stop-codons
• 2557 (or 12%) high-confidence genes
has a stop-codon in ≥1line
• 870 genes have a segregating stop-
codon in ≥ 2 of improved lines
Chia et al. Submitted
Artificial selection across the maize genome
HISTORICAL GENOMICS OF MAIZE






3
%





3


3
%
02




%
22222222222222222222222222222222222222222222222222222222222222200000000000000000000000000000000222222000022022222022200000000000000000000000000000000000000000000000000000000000000000022222200000000000000000000000020000000
%
2+
Spatial resolution -- genome resequencing
Temporal resolution -- SNP genotyping
Detailed historical look at selection during
modern breeding
• Larger sample size
• Increased chronological
resolution
• Take into account heterotic
group structure
• Focus on corn belt varieties
Resolve caveats of
resequencing approach
Genotyping and Sampling
• 400 N.American corn belt lines
• Genotype on public Illumina 55K
• Tracked population structure,
ancestry, and selection over time
99
94
70
137
land races
1950 inbreds
1960-1970 inbreds
ex-PVP
0
1
2
3
van Heerwaarden et al. Submitted
(Oh43,W22, B14)
(B73, 207, Mo17)
Population structure through time
van Heerwaarden et al. Submitted
Population structure through time
van Heerwaarden et al. Submitted
C
Population structure through time
van Heerwaarden et al. Submitted
C
C
Population structure through time
van Heerwaarden et al. Submitted
C
C
Population structure through time
van Heerwaarden et al. Submitted
C
C
Population structure through time
van Heerwaarden et al. Submitted
Iodent
NSS
SS
Number and diversity of ancestors decreases
through time
ancestry
van Heerwaarden et al. Submitted
c.
Iodent
NSS
SS
effective#ancestorsdiversityofancestors
SS
0.0
0.1
0.2
0.3
0.4
undefined
OH43
CI31A
HY
B8
B10
B14
B96
B37
I205
OH07
CI3A
CI187-2
CI540
I224
WD456
Oh3167B
Tr9-1-1-6
FE2
LE773
ND203
B73
A634
A635
N28
H100
B64
B14A
B68
CM105
B84
A632
N196
LH195
LH205
LH196
LH194
991
LH74
PHG39
LH132
G80
78004
78010
4676A
78002A
794
LP5
PHT55
H8431
1 2 3
Ancestral contributions of individual lines
Ancestral contributions of individual lines
IDT
1 2 3
0.0
0.1
0.2
0.3
0.4
undefined
OH43
WF9
A375
A509
A556
I198
B2
H5
HY
B164
G
ND203
B10
B14
L317
I205
CI187-2
C49A
I224
AH83
Tr9-1-1-6
C11
IDT
A638
M14
207
PHN34
PHP76
PHW86
PHG50
PHG35
PHG71
IB014
PHG83
LH150
PHG29
PHG72
PHG84
PHZ51
PHV78
PHK42
PHN11
PHH93
PHJ33
PHN73
PHR62
Weak landrace structure still evident in modern inbreds
ancestryproportion
Iodent
NSS
SS
Selection and frequency over time
Duvick et al. 2004 Plant Breeding Reviews
advantageous alleles show continual increase
in frequency over time
•Identify genetic structure across all time periods
(PCA,Tracy-Widom)
•Treat time period as a phenotype for association
mapping
•For each SNP, compare two models:
•M0: Frequency determined by drift and population
structure (covariance matrix of all SNPs)
•M1: Frequency determined by drift, population
structure AND environment (time)
•Bayes Factor for each SNP
Time as a phenotype to identify selection
0
1
2
3
Coop et al. 2010 Genetics
Temporal association identifies candidates of selection
• 236 Candidate regions (1021 genes) with consistent BF across runs
• Include stress response, lignin biosynthesis, auxin response
• Two of the top candidates ZmErecta (US7847158) and ZmArgos
(US7834240) patented for plant growth, yield
ssociation identifies candidates
te regions (1021 genes) with consistent BF
0 1 2 3
0.00.20.40.60.81.0
era
p
Temporal association identifies candidates of selection
• 236 Candidate regions (1021 genes) with consistent BF across runs
• Include stress response, lignin biosynthesis, auxin response
• Two of the top candidates ZmErecta (US7847158) and ZmArgos
(US7834240) patented for plant growth, yield
Diversity
Genome Sequence
Selective Sweep
Selective sweeps
No abnormal haplotypes, ancestry at selected sites
0 1 2 3
01234
p p p p p p p p
era
ratioobserved/randomized
No abnormal haplotypes, ancestry at selected sites
Genome-wide ancestry not determined by selection
Weak correlation between good alleles and
contribution to modern lines
1950’s inbreds
1980’s inbreds
ex-PVP lines
selected regions
%ancestry
Weak correlation between good alleles and
contribution to modern lines
Structure and selection in corn belt maize
Some final thoughts on adaptation...
modern corn
phenotypic
space
FISHER-ORR MODEL OF ADAPTATION
modern corn teosinte
phenotypic
space
FISHER-ORR MODEL OF ADAPTATION
modern corn teosinte
phenotypic
space
FISHER-ORR MODEL OF ADAPTATION
landraces
phenotypic
space
FISHER-ORR MODEL OF ADAPTATION
landraces
phenotypic
space
FISHER-ORR MODEL OF ADAPTATION
Brown et al. 2011 PLoS Genetics
• Effect sizes of ear vs. other
consistent with Fisher-Orr
model
• Larger effects → larger fitness
difference → stronger selection
ThankYou!

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Historical Genomics of US Maize: Domestication and Modern Breeding

  • 1. Genome-Wide View of Breeding History and Selection in North American Maize Dr. Jeffrey Ross-Ibarra University of California at Davis Patterns of diversity across the genome are reflective of the historical processes of selection, drift, and mutation that have acted on a species during its evolution. Here, we apply population genetic analysis of two genomic datasets to assess the spatial and temporal signatures of evolution in the maize genome. We first describe genome-wide patterns of evolution during two epochs of selection, domestication and modern breeding, using full-genome resequencing of a number of maize and teosinte lines. Then, using a chronologically-stratified panel of corn belt lines, we dissect temporal patterns of ancestry and selection in greater detail across the 80+ years of North American corn breeding. We find distinct impacts of selection during domestication and modern breeding on diversity and gene expression, identify candidate regions targeted by selection, and describe changes in genetic structure and ancestry during the evolution of modern corn belt lines.
  • 2. HISTORICAL GENOMICS OF MAIZE Jeffrey Ross-Ibarra www.rilab.org
  • 3. Acknowledgements Ed Buckler (Cornell, USDA) Jeff Glaubitz (Cornell) Major Goodman (NC State) Mike McMullen (Missouri, USDA) Chi Song (BGI) Nathan Springer (Minnesota) Doreen Ware (CSHL, USDA) Xun Xu (BGI) Matthew Hufford Joost van Heerwaarden Tanja Pyhäjärvi Jer-Ming Chia
  • 4. HISTORICAL GENOMICS OF MAIZE 3 % 3 3 % 02 % 22222222222222222222222222222222222222222222222222222222222222200000000000000000000000000000000222222000022022222022200000000000000000000000000000000000000000000000000000000000000000022222200000000000000000000000020000000 % 2+ Spatial resolution -- genome resequencing Temporal resolution -- SNP genotyping
  • 5. HISTORICAL GENOMICS OF MAIZE 3 % 3 3 % % 2222222222222222222222222222222222222222222222222000000000000000000022022020020222200200000000000000000000000000000000000000222220000000000000000020000000 % 2+ Spatial resolution -- genome resequencing Temporal resolution -- SNP genotyping
  • 6. ρ 0.0020.0060.01 00.010.020.030.04 ρρ ππ lower 1% cent10 cM/Mb ρ Chr 10 Maize Hapmap I: low-copy fraction of genome Gore et al. 2009 Science • Re-sequenced low-copy portion of genome of 27 inbreds • High diversity genome, but large regions of low recombination • Identified low diversity putative targets of selection • No comparison to older material • Cannot distinguish domestication from modern improvement
  • 7. Chia et al. Submitted Maize Hapmap II: full genome resequencing 75 resequenced genomes 21M SNPs75 resequenced genomes 21M SNPs Sequenced Genomes Sequence Depth Locality Improved 35 5.04 X 13 Temperate, 13 Tropical, 3 Mixed, 6 Chinese Landraces 23 5.34 X 9 South American, 14 North American parviglumis 14 3.81 X 4 Jalisco/Nayarit, 9 Balsas, 1 Oaxaca 1 1Oaxaca mexicana 2 6.83 X 1 Jalisco, 1 Morelos Tripsacum 1 12.62 X Colombia parviglumis Landraces Improved Lines Domestication Improvement Hufford et al. Submitted
  • 8. Maize Parviglumis Maize Parviglumis Genic Tajima's D Tajima's D Density -4 -2 0 2 4 0.00.10.20.30.40.5 Hufford et al. Submitted
  • 9. Maize Parviglumis Maize Parviglumis Genic Tajima's D Tajima's D Density -4 -2 0 2 4 0.00.10.20.30.40.5 Density 0.00.10.20.30.40.5 Genome-wide Tajima's D Tajima's D Density -4 -2 0 2 4 0.00.10.20.30.4 Hufford et al. Submitted
  • 10. Chen et al. 2010 Genome Research COG3-like FMP25-like frq PAC10-like SEC14-like NSL1-like NCU02261 B Carib LA Out Ellison et al. 2011 PNAS • Cross-Population Composite Likelihood Ratio • Identifies extended regions of differentiation • Compares to simulated model • Define selected regions, estimate s
  • 11. Artificial selection in the maize genome • Stronger selection during domestication (s~0.015 vs. s~0.003) • Selection strength consistent with archaeology natural selection • Continued selection on domestication genes (18% overlap) • ~3,000 genes in selected regions. Identified ~1100 candidates • 5-10% of selected regions had no genes Hufford et al. Submitted he maize genome log s Frequency -6 -5 -4 -3 -2 050001500025000 domestication improvement
  • 12. Gore et al. Science 2009 Mb chr 8 proportion FST Mb chr 8 proportion 0.00.20.40.60.81.0 fixed shared unique temperate unique tropicalemfixed shared unique temperate unique tropical 0 20 40 60 80 100 120 140 160 180 00.050.150.250.35 Population-specific selection
  • 13. Population-specific selection Hufford et al. Submitted • Many population-specific loci • Stronger overall estimate of selection • Still weaker than domestication • Lower power to rule out drift
  • 14. Candidate genes for maize improvement Hufford et al. Submitted
  • 15. Selection on the transcriptome • Expression at 18K genes of 27 maize and teosinte using Nimblegen array • Domestication directly selected on candidate gene expression • Breeding has worked with highly expressed genes • Modern breeding selected for heterosis in expression Candidates: DOM IMP Change in expression * -- Decreased variance * * Tissue specificity# -- overall higher expression Dominance in crosses# -- inter intra # Data from Stupar et al. 2008 BMC Plant Bio; Sekhon et al. 2011 Plant J. Hufford et al. Submitted
  • 16. Regions with no genes likely regulatory teosintemaize Swanson-Wagner et al. Submitted Expression
  • 17. Genetic load in modern maize • ~1% of SNPs disrupts predicted protein • 10,117 premature stop-codons • 2557 (or 12%) high-confidence genes has a stop-codon in ≥1line • 870 genes have a segregating stop- codon in ≥ 2 of improved lines Chia et al. Submitted
  • 18.
  • 19.
  • 20. Artificial selection across the maize genome
  • 21. HISTORICAL GENOMICS OF MAIZE 3 % 3 3 % 02 % 22222222222222222222222222222222222222222222222222222222222222200000000000000000000000000000000222222000022022222022200000000000000000000000000000000000000000000000000000000000000000022222200000000000000000000000020000000 % 2+ Spatial resolution -- genome resequencing Temporal resolution -- SNP genotyping
  • 22. Detailed historical look at selection during modern breeding • Larger sample size • Increased chronological resolution • Take into account heterotic group structure • Focus on corn belt varieties Resolve caveats of resequencing approach
  • 23. Genotyping and Sampling • 400 N.American corn belt lines • Genotype on public Illumina 55K • Tracked population structure, ancestry, and selection over time 99 94 70 137 land races 1950 inbreds 1960-1970 inbreds ex-PVP 0 1 2 3 van Heerwaarden et al. Submitted (Oh43,W22, B14) (B73, 207, Mo17)
  • 24. Population structure through time van Heerwaarden et al. Submitted
  • 25. Population structure through time van Heerwaarden et al. Submitted C
  • 26. Population structure through time van Heerwaarden et al. Submitted C C
  • 27. Population structure through time van Heerwaarden et al. Submitted C C
  • 28. Population structure through time van Heerwaarden et al. Submitted C C
  • 29. Population structure through time van Heerwaarden et al. Submitted Iodent NSS SS
  • 30. Number and diversity of ancestors decreases through time ancestry van Heerwaarden et al. Submitted c. Iodent NSS SS effective#ancestorsdiversityofancestors
  • 32. Ancestral contributions of individual lines IDT 1 2 3 0.0 0.1 0.2 0.3 0.4 undefined OH43 WF9 A375 A509 A556 I198 B2 H5 HY B164 G ND203 B10 B14 L317 I205 CI187-2 C49A I224 AH83 Tr9-1-1-6 C11 IDT A638 M14 207 PHN34 PHP76 PHW86 PHG50 PHG35 PHG71 IB014 PHG83 LH150 PHG29 PHG72 PHG84 PHZ51 PHV78 PHK42 PHN11 PHH93 PHJ33 PHN73 PHR62
  • 33. Weak landrace structure still evident in modern inbreds ancestryproportion Iodent NSS SS
  • 34. Selection and frequency over time Duvick et al. 2004 Plant Breeding Reviews advantageous alleles show continual increase in frequency over time
  • 35. •Identify genetic structure across all time periods (PCA,Tracy-Widom) •Treat time period as a phenotype for association mapping •For each SNP, compare two models: •M0: Frequency determined by drift and population structure (covariance matrix of all SNPs) •M1: Frequency determined by drift, population structure AND environment (time) •Bayes Factor for each SNP Time as a phenotype to identify selection 0 1 2 3 Coop et al. 2010 Genetics
  • 36. Temporal association identifies candidates of selection • 236 Candidate regions (1021 genes) with consistent BF across runs • Include stress response, lignin biosynthesis, auxin response • Two of the top candidates ZmErecta (US7847158) and ZmArgos (US7834240) patented for plant growth, yield ssociation identifies candidates te regions (1021 genes) with consistent BF 0 1 2 3 0.00.20.40.60.81.0 era p
  • 37. Temporal association identifies candidates of selection • 236 Candidate regions (1021 genes) with consistent BF across runs • Include stress response, lignin biosynthesis, auxin response • Two of the top candidates ZmErecta (US7847158) and ZmArgos (US7834240) patented for plant growth, yield
  • 39. No abnormal haplotypes, ancestry at selected sites 0 1 2 3 01234 p p p p p p p p era ratioobserved/randomized
  • 40. No abnormal haplotypes, ancestry at selected sites
  • 41. Genome-wide ancestry not determined by selection
  • 42. Weak correlation between good alleles and contribution to modern lines 1950’s inbreds 1980’s inbreds ex-PVP lines selected regions %ancestry
  • 43. Weak correlation between good alleles and contribution to modern lines
  • 44. Structure and selection in corn belt maize
  • 45. Some final thoughts on adaptation...
  • 51. Brown et al. 2011 PLoS Genetics • Effect sizes of ear vs. other consistent with Fisher-Orr model • Larger effects → larger fitness difference → stronger selection