Langebio 2015

Selection and demography in maize evolution

Jeffrey Ross-Ibarra @jrossibarra • www.rilab.org

Dept. Plant Sciences • Center for Population Biology • Genome Center University of California Davis

photo by lady_lbrty

Photos: Matt Hufford, Brandon Gaut, John Doebley

maizeteosinte

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tHake & Ross-Ibarra 2015 eLife

hard sweepD

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hard sweep multiple mutations

Div

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ystanding variation

“soft” sweeps

hard sweep multiple mutations polygenic adaptation

Div

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ystanding variation

“soft” sweeps

M T G P H R L

GGTCGAC ATG ACT GGT CCA CAT CGA CTG TAG

M T G P H R L

GGTCGAC ATG ACT GGT CCA CAT CGA CTG TAG

M T N P H R L

GGTCGAC ATG ACT GAT CCA CAT CGA CTG TAG

M T G P H R L

GGTAAAC ATG ACT GGT CCA CAT CGA CTG TAG

GG—-AC ATG ACT GGT CCA CAT CGA CTG TAG

Meyerowitz 1994 Current Biology Duvick et al. 1999 US 6639132 B1

maize origins

Tripsacum extinct maizeF1F1

teosinte (Z. mays ssp. parviglumis)

maize (Z. mays ssp. mays)

F1

Beadle 1979 Field Museum of Nat. Hist. Bull.

F1


F1


F1


Briggs et al. 2007 Genetics

1 2 3 4 5

6 7 8 9 10

Wang et al. 2005 Nature

1 2 3 4 5

6 7 8 9 10

Figure 1.Phenotypes. a. Maize ear showing the cob (cb) exposed at top. b. Teosinte ear with the rachisinternode (in) and glume (gl) labeled. c. Teosinte ear from a plant with a maize allele of tga1introgressed into it. d. Close-up of a single teosinte fruitcase. e. Close-up of a fruitcase fromteosinte plant with a maize allele of tga1 introgressed into it. f. Ear of maize inbred W22(Tga1-maize allele) with the cob exposed showing the small white glumes at the base. g. Earof maize inbred W22:tga1 which carries the teosinte allele, showing enlarged (white) glumes.h. Ear of maize inbred W22 carrying the tga1-ems1 allele, showing enlarged glumes. For highermagnification copies of f–h see Supplementary Information.

Wang et al. Page 10

Nature. Author manuscript; available in PMC 2006 May 23.

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Wang et al. 2015 Genetics

Wang et al. 2005 Nature

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Figure 1.Phenotypes. a. Maize ear showing the cob (cb) exposed at top. b. Teosinte ear with the rachisinternode (in) and glume (gl) labeled. c. Teosinte ear from a plant with a maize allele of tga1introgressed into it. d. Close-up of a single teosinte fruitcase. e. Close-up of a fruitcase fromteosinte plant with a maize allele of tga1 introgressed into it. f. Ear of maize inbred W22(Tga1-maize allele) with the cob exposed showing the small white glumes at the base. g. Earof maize inbred W22:tga1 which carries the teosinte allele, showing enlarged (white) glumes.h. Ear of maize inbred W22 carrying the tga1-ems1 allele, showing enlarged glumes. For highermagnification copies of f–h see Supplementary Information.

Wang et al. Page 10

Nature. Author manuscript; available in PMC 2006 May 23.

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tga1

Wang et al. 2015 Genetics

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gt1 tga1

Wills et al. 2013 PLoS Genetics

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6 7 8 9 10

gt1 tga1


teosinte maizeClint Whipple, BYU

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gt1 tga1


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gt1 tga1


5’ control region 3’ UTR

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tb1

Studer et al. 2011 Nat. Gen.; Vann et al. 2015 PeerJ

tga1gt1

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NATURE GENETICS ADVANCE ONLINE PUBLICATION 3

L E T T E R S

mutation rate21, strongly suggesting that the Hopscotch insertion (and thus, the older Tourist as well) existed as standing genetic variation in the teosinte ancestor of maize. Thus, we conclude that the Hopscotch insertion likely predated domestication by more than 10,000 years and the Tourist insertion by an even greater amount of time.

We identified four fixed differences in the portion of the proximal and distal components of the control region that show evidence of selection. We used transient assays in maize leaf protoplasts to test all four differences for effects on gene expression. Maize and teosinte chromosomal segments for the portions of the proximal and distal components with these four differences were cloned into reporter constructs upstream of the minimal promoter of the cauliflower mosaic virus (mpCaMV), the firefly luciferase ORF and the nopaline synthase (NOS) terminator (Fig. 4). Each construct was assayed for luminescence after transformation by electroporation into maize pro-toplast. The constructs for the distal component contrast the effects of the Tourist insertion plus the single fixed nucleotide substitution that distinguish maize and teosinte. Both the maize and teosinte constructs for the distal component repressed luciferase expression

relative to the minimal promoter alone. The maize construct with Tourist excised gave luciferase expression equivalent to the native maize and teosinte constructs and less expression than the minimal promoter alone. These results indicate that this segment is function-ally important, acting as a repressor of luciferase expression and, by inference, of tb1 expression in vivo. However, we did not observe any difference between the maize and teosinte constructs as anticipated. One possible cause for the lack of differences in expression between the maize and teosinte constructs might be that additional proteins required to cause these differences are not present in maize leaf pro-toplast. Another possibility is that the factor affecting phenotype in the distal component lies in the unselected region between −64.8 and −69.5 kb, which is not included in the construct. Nevertheless, the results do indicate that the distal component has a functional element that acts as a repressor. The functional importance of this segment is supported by its low level of nucleotide diversity (Fig. 3a), suggesting a history of purifying selection.

The constructs for the proximal component of the control region contrast the effects of the Hopscotch insertion plus a single fixed nucleo-tide substitution that distinguish maize and teosinte. The construct with the maize sequence including Hopscotch increased expression of the luciferase reporter twofold relative to the teosinte construct for the proximal control region and the minimal promoter alone (Fig. 4). Luciferase expression was returned to the level of the teosinte con-struct and the minimal promoter construct by deleting the Hopscotch element from the full maize construct. These results indicate that the Hopscotch element enhances luciferase expression and, by

a

b

0.06

A B C D M

T

P = 0.95 P = 0.41 P = 0.04

HKA neutrality tests

P 0.0001

0.04

0.02

0–67 kb –66 kb

Distalcomponent

Teosinte clusterhaplotype

Maize clusterhaplotype

Proximalcomponent

–65 kbTourist408 bp

Hopscotch4,885 bp

–64 kb –58 kb

Figure 3 Sequence diversity in maize and teosinte across the control region. (a) Nucleotide diversity across the tb1 upstream control region. Base-pair positions are relative to AGPv2 position 265,745,977 of the maize reference genome sequence. P values correspond to HKA neutrality tests for regions A–D, as defined by the dotted lines. Green shading signifies evidence of neutrality, and pink shading signifies regions of non-neutral evolution. Nucleotide diversity ( ) for maize (yellow line) and teosinte (green line) were calculated using a 500-bp sliding window with a 25-bp step. The distal and proximal components of the control region with four fixed sequence differences between the most common maize haplotype and teosinte haplotype are shown below. (b) A minimum spanning tree for the control region with 16 diverse maize and 17 diverse teosinte sequences. Size of the circles for each haplotype group (yellow, maize; green, teosinte) is proportional to the number of individuals within that haplotype.

Transient assay constructs

mpCaMV luc

luc

luc

luc

luc

luc

luc

luc

Hopscotch

Tourist

mpCaMV

T-dist

M-dist

T-prox

M-prox

0 0.5 1.0 1.5 2.0

∆M-dist

∆M-proxPro

xim

al c

ontr

ol r

egio

nD

ista

l con

trol

reg

ion

Relative expression

Figure 4 Constructs and corresponding normalized luciferase expression levels. Transient assays were performed in maize leaf protoplast. Each construct is drawn to scale. The construct backbone consists of the minimal promoter from the cauliflower mosaic virus (mpCaMV, gray box), luciferase ORF (luc, white box) and the nopaline synthase terminator (black box). Portions of the proximal and distal components of the control region (hatched boxes) from maize and teosinte were cloned into restriction sites upstream of the minimal promoter. “ ” denotes the excision of either the Tourist or Hopscotch element from the maize construct. Horizontal green bars show the normalized mean with s.e.m. for each construct.

relative expressionconstruct

gt1

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6 7 8 9 10

tb1Figure 2 Map of parviglumis Populations and Hopscotch allele frequency. Map showing the frequencyof the Hopscotch allele in populations of parviglumis where we sampled more than 6 individuals. Size ofcircles reflects number of individuals sampled. The Balsas River is shown, as the Balsas River Basin isbelieved to be the center of domestication of maize.

as our independent trait for phenotyping analyses. SAS code used for analysis is available athttp://dx.doi.org/10.6084/m9.figshare.1166630.

RESULTSGenotyping for the Hopscotch insertionThe genotype at the Hopscotch insertion was confirmed with two PCRs for 837 individualsof the 1,100 screened (Table S1 and Table S2). Among the 247 maize landrace accessionsgenotyped, all but eight were homozygous for the presence of the insertion Withinour parviglumis and mexicana samples we found the Hopscotch insertion segregatingin 37 (n = 86) and four (n = 17) populations, respectively, and at highest frequencywithin populations in the states of Jalisco, Colima, and Michoacan in central-westernMexico (Fig. 2). Using our Hopscotch genotyping, we calculated diVerentiation betweenpopulations (FST) and subspecies (FCT) for populations in which we sampled sixteenor more chromosomes. We found that FCT = 0, and levels of FST among populationswithin each subspecies (0.22) and among all populations (0.23) (Table 1) are similar togenome-wide estimates from previous studies Pyhajarvi, HuVord & Ross-Ibarra, 2013.Although we found large variation in Hopscotch allele frequency among our populations,BayEnv analysis did not indicate a correlation between the Hopscotch insertion andenvironmental variables (all Bayes Factors < 1).

Vann et al. (2015), PeerJ, DOI 10.7717/peerj.900 8/21


tga1

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11 N

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NATURE GENETICS ADVANCE ONLINE PUBLICATION 3

L E T T E R S

mutation rate21, strongly suggesting that the Hopscotch insertion (and thus, the older Tourist as well) existed as standing genetic variation in the teosinte ancestor of maize. Thus, we conclude that the Hopscotch insertion likely predated domestication by more than 10,000 years and the Tourist insertion by an even greater amount of time.

We identified four fixed differences in the portion of the proximal and distal components of the control region that show evidence of selection. We used transient assays in maize leaf protoplasts to test all four differences for effects on gene expression. Maize and teosinte chromosomal segments for the portions of the proximal and distal components with these four differences were cloned into reporter constructs upstream of the minimal promoter of the cauliflower mosaic virus (mpCaMV), the firefly luciferase ORF and the nopaline synthase (NOS) terminator (Fig. 4). Each construct was assayed for luminescence after transformation by electroporation into maize pro-toplast. The constructs for the distal component contrast the effects of the Tourist insertion plus the single fixed nucleotide substitution that distinguish maize and teosinte. Both the maize and teosinte constructs for the distal component repressed luciferase expression

relative to the minimal promoter alone. The maize construct with Tourist excised gave luciferase expression equivalent to the native maize and teosinte constructs and less expression than the minimal promoter alone. These results indicate that this segment is function-ally important, acting as a repressor of luciferase expression and, by inference, of tb1 expression in vivo. However, we did not observe any difference between the maize and teosinte constructs as anticipated. One possible cause for the lack of differences in expression between the maize and teosinte constructs might be that additional proteins required to cause these differences are not present in maize leaf pro-toplast. Another possibility is that the factor affecting phenotype in the distal component lies in the unselected region between −64.8 and −69.5 kb, which is not included in the construct. Nevertheless, the results do indicate that the distal component has a functional element that acts as a repressor. The functional importance of this segment is supported by its low level of nucleotide diversity (Fig. 3a), suggesting a history of purifying selection.

The constructs for the proximal component of the control region contrast the effects of the Hopscotch insertion plus a single fixed nucleo-tide substitution that distinguish maize and teosinte. The construct with the maize sequence including Hopscotch increased expression of the luciferase reporter twofold relative to the teosinte construct for the proximal control region and the minimal promoter alone (Fig. 4). Luciferase expression was returned to the level of the teosinte con-struct and the minimal promoter construct by deleting the Hopscotch element from the full maize construct. These results indicate that the Hopscotch element enhances luciferase expression and, by

a

b

0.06

A B C D M

T

P = 0.95 P = 0.41 P = 0.04

HKA neutrality tests

P 0.0001

0.04

0.02

0–67 kb –66 kb

Distalcomponent

Teosinte clusterhaplotype

Maize clusterhaplotype

Proximalcomponent

–65 kbTourist408 bp

Hopscotch4,885 bp

–64 kb –58 kb

Figure 3 Sequence diversity in maize and teosinte across the control region. (a) Nucleotide diversity across the tb1 upstream control region. Base-pair positions are relative to AGPv2 position 265,745,977 of the maize reference genome sequence. P values correspond to HKA neutrality tests for regions A–D, as defined by the dotted lines. Green shading signifies evidence of neutrality, and pink shading signifies regions of non-neutral evolution. Nucleotide diversity ( ) for maize (yellow line) and teosinte (green line) were calculated using a 500-bp sliding window with a 25-bp step. The distal and proximal components of the control region with four fixed sequence differences between the most common maize haplotype and teosinte haplotype are shown below. (b) A minimum spanning tree for the control region with 16 diverse maize and 17 diverse teosinte sequences. Size of the circles for each haplotype group (yellow, maize; green, teosinte) is proportional to the number of individuals within that haplotype.

Transient assay constructs

mpCaMV luc

luc

luc

luc

luc

luc

luc

luc

Hopscotch

Tourist

mpCaMV

T-dist

M-dist

T-prox

M-prox

0 0.5 1.0 1.5 2.0

∆M-dist

∆M-proxPro

xim

al c

ontr

ol r

egio

nD

ista

l con

trol

reg

ion

Relative expression

Figure 4 Constructs and corresponding normalized luciferase expression levels. Transient assays were performed in maize leaf protoplast. Each construct is drawn to scale. The construct backbone consists of the minimal promoter from the cauliflower mosaic virus (mpCaMV, gray box), luciferase ORF (luc, white box) and the nopaline synthase terminator (black box). Portions of the proximal and distal components of the control region (hatched boxes) from maize and teosinte were cloned into restriction sites upstream of the minimal promoter. “ ” denotes the excision of either the Tourist or Hopscotch element from the maize construct. Horizontal green bars show the normalized mean with s.e.m. for each construct.

relative expressionconstruct

gt1

hard sweep

M T N P H R L

GGTCGA ATG ACT GAT CCA CAT CGA CTG TAG

tga1

hard sweep

M T N P H R L

GGTCGA ATG ACT GAT CCA CAT CGA CTG TAG

tga1 gt1 tb1

Multiple Mutations

Standing Variation

M T G P H R L

GGTAAA ATG ACT GGT CCA CAT CGA CTG TAG

Vann et al. 2015 PeerJ

polygenic adaptation

30% phenotypic variance

0% phenotypic variance

Hufford et al. 2012 Nat. Gen. Chia et al. 2012 Nat. Gen

13 teosinte 23 maize

~500 genes (2%) 11M shared SNPs

3,000 fixed genomes:


13 teosinte 23 maizegenomes:


13 teosinte 23 maizegenomes:

Swanson-Wagner et al. 2012 PNAS

whereas others are lost after domestication (Fig. 3B). It should benoted that many of these genes have unique coexpression edges inmaize that are not observed in teosinte (Fig. S4B).

Expression data provide an opportunity to investigate furtherfunctional alterations to genes located within genomic regionsthat population genomic analyses identify as targets of selective

E

DE(n=612)

AEC(n=1115)

Dom/Imp genes(n=1761)

292 230750

894644

1582

A

B

Teosinte network edges Maize network edges

D

C

GRMZM2G068436

GRMZM2G137947

GRMZM2G375302

Mb

Mb

Fig. 3. Analysis of genes with altered expression or conservation and targets of selection during improvement and/or domestication. (A) Venn diagramshowing the overlap between DE genes, AEC genes, and the genes that occur in genomic regions that have evidence for selective sweeps during maizedomestication or improvement (Dom/Imp genes). (B) Teosinte coexpression networks for three genes (GRMZM2G068436, GRMZM2G137947, andGRMZM2G375302). (Right) Edges that are maintained in maize coexpression networks are shown. Although the differentially expressed gene (red node) ishighly connected in teosinte, most of these connections are lost in maize. However, some parts of the teosinte network are still conserved in maize. (C) Cross-population composite likelihood ratio test (XP-CLR) plot shows the evidence for a selective sweep that occurs on chromosome 9. The tick marks along the xaxis represent genes, and the red tick mark indicates the gene (GRMZM2G448355) that was chosen as the candidate target of selection and is differentiallyexpressed in maize and teosinte. The bar plot underneath the graph shows the expression levels of all maize (blue) and teosinte (red) samples. (D) XP-CLR plotfor a large region on chromosome 5. The candidate target of selection is indicated in green and shows similar expression in maize and teosinte. Two othergenes (red) exhibit DE. (E) Neighbor-joining tree shows the relationships among the haplotypes at GRMZM2G141858. (Right) Bar plot shows expression levelsfor each genotype; red bars indicate teosinte genotypes, and blue bars represent maize genotypes. At least one teosinte genotype (TIL15) contains thehaplotype that has been selected in maize and has expression levels similar to maize genotypes.

Table 2. Genes in selected regions with evidence for DE or AEC

Gene listNo. genes selectedduring dom/imp

% up-regulatedin maize Significance

% higher connectedin maize % candidates

AEC and DE (n = 276) 46 76 0.0002 41.3 39.1DE only (n = 336) 44 61 0.0230 40.9 22.7AEC only (n = 839) 89 54 0.1837 57.3 32.6

dom, domestication; imp, improvement.

4 of 6 | www.pnas.org/cgi/doi/10.1073/pnas.1201961109 Swanson-Wagner et al.

ExpressionGenealogy

teosintemaize

nucl

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distance to nearest substitution (cM)

Beissinger et al. In Prep: http://biorxiv.org/content/early/

http://biorxiv.org/content/early/2015/11/13/031666

nucl

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Mexico lowland

9,000 BP

Matsuoka et al. 2002; Piperno 2006 Perry et al. 2006; Piperno et al. 2009

Mexico highland6,000 BP

Mexico lowland

9,000 BP



S. America lowland

6,000 BP

Mexico lowland

9,000 BP



S. America lowland

6,000 BP

S. America Highland

4,000 BP

Mexico lowland

9,000 BP


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Tassel Br. Number

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SA MEX SA MEX

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95 landraces ~100K SNPs

Takuno et al. 2015 Genetics

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unique S. America

unique Mexico

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39%61%

IntergenicGenic

19%

81%

Standing VariationNew mutation


Beissinger et al. In Prep (b) Berg & Coop 2014 PLoS Genetics


Z =LX

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allele freq.population breeding value

effect size


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how to adapt: Zea mays

soft sweeps

M T G P H R L

GGTAAA ATG ACT GGT CCA CAT CGA CTG TAG

polygenic adaptation

regulatory variation

Sattah et al. 2011 PLoS Gen. Williamson et al. 2014 PLoS Gen Hernandez et al. 2011 Science



dive

rsity

Ne diploids

s selection coefficient

selection is effective if 2Nes > 1

Ne diploids



Ne ~ 150,000 Ne ~ 10,000

Ne ~ 2,000,000 Ne ~ 600,000

Ne diploids



Ne ~ 150,000 Ne ~ 10,000

Ne ~ 2,000,000 Ne ~ 600,000

20% nonsyn. subs 10% nonsyn. subs

50% nonsyn. subs 40% nonsyn. subs

teos

inte

maize

DATAte

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MODEL

Beissinger et al. In Prep: http://biorxiv.org/content/early/2015/11/13/031666 Hufford et al. 2012


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MODEL

0.05Na

Na

Na 3Na

Beissinger et al. In Prep: http://biorxiv.org/content/early/2015/11/13/031666 Hufford et al. 2012


Ne ~ 150,000

Ne ~ 50,000



0.05Na

Na

Na 3NaNe ~ 450,000



0.05Na

Na

Na 3NaNe ~ 450,000

Ne ~ 1,000,000



0.05Na

Na

Na 3NaNe ~ 450,000

Ne ~ 1,000,000

1e+05

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1e+09

1e+03 1e+042e+04 1e+05years(u=3e−8, generation=1)

effe

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size

popBKN_4HapBKN_6HapTIL_4Hap_JaliscoTIL_6Hap

Ne ~ 1,000,000,000



0.05Na

Na

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Ne ~ 1,000,000

1e+05

1e+07

1e+09

1e+03 1e+042e+04 1e+05years(u=3e−8, generation=1)

effe

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pop

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size

popBKN_4HapBKN_6HapTIL_4Hap_JaliscoTIL_6Hap

Ne ~ 1,000,000,000

Ne ~ 5,000,000,000



nucl

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distance to gene (cM)



nucl

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sing

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sing

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dive

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Ne >> 1,000,000 Ne ~ 10,000*

Ne ~ 2,000,000 Ne ~ 600,000

M T G P H R L

ATG ACT GGT CCA CAT CGA CTG TAG

M T G P H R L


M T N P H R L

ATG ACT GAT CCA CAT CGA CTG TAGx

M T G P H R L


M T N P H R L

ATG ACT GAT CCA CAT CGA CTG TAGx

M T G P H R L


M T N P H R L

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x x x

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x xx x

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Makarevitch et al. 2014 PLoS Genetics


single TE family, many genes


single TE family, many genes

new insertions activate expression

Makarevitch et al. 2014 bioRxiv

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0.5

1.5

2.5

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Lines without the TE insertion

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***

****

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single gene, many individuals

Hancock et al 2011 Science Hernandez et al. 2011 Science

Fraser et al. 2013 Gen. Research

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µ beneficial mutation rate per trait

selection from standing variation when 2Neµ > 1

Ne diploids



Garud et al. 2015 PLoS Gen. Jensen 2014 Nat. Comm.

Pritchard et al. 2010 Curr. Bio. Enard et al. 2014 Gen. Res.

Beissinger et al. In Prep

µ ∝ 2,500 Mbp µ ∝ 3,100 Mbp

µ ∝ 130 Mbp

Ne diploids



Garud et al. 2015 PLoS Gen. Jensen 2014 Nat. Comm.

Pritchard et al. 2010 Curr. Bio. Enard et al. 2014 Gen. Res.

Beissinger et al. In Prep

µ ∝ 2,500 Mbp µ ∝ 3,100 Mbp

µ ∝ 130 Mbp µ ∝ 220 Mbp

µ ∝ 130 Mbp

Williamson et al. 2014 PLoS Gen

Brandon Gaut

maizeArabidopsisKew C-Value Database

log 1C genome size

• “Soft sweeps” and polygenic selection predominate in maize and teosinte

• Most selection appears in noncoding sequence

• Both effective population size & mutational target contribute

• Large, complex genomes may mean more targets & more soft sweeps & less linked effects of selection

Concluding Thoughts

Acknowledgments

Maize Diversity GroupPeter Bradbury

Ed Buckler John Doebley Theresa Fulton

Sherry Flint-GarciaJim Holland

Sharon Mitchell Qi Sun

Doreen Ware

CollaboratorsGraham Coop

Nathan Springer Ruairidh Sawers

Lab AlumniTim Beissinger (USDA-ARS, Mizzou)

Kate Crosby (Monsanto) Matt Hufford (Iowa State)

Tanja Pyhäjärvi (Oulu) Shohei Takuno (Sokendai)

Joost van Heerwaarden (Wageningen)