Genome-wide genetic changes during modern breeding of maize · 2017-03-13 · Elite Chinese chang7-2 24.95 Elite Chinese dan340 7.05 Elite Chinese danhuang02 6.34 Elite Chinese lv28

NATURE GENETICS

CORRECT ION NOT ICE

Nat. Genet. 44, 812–815 (2012); published online 3 June 2012; corrected online 27 August 2014

Genome-wide genetic changes during modern breeding of maizeYinping Jiao, Hainan Zhao, Longhui Ren, Weibin Song, Biao Zeng, Jinjie Guo, Baobao Wang, Zhipeng Liu, Jing Chen, Wei Li, Mei Zhang, Shaojun Xie & Jingsheng LaiIn the version of this supplementary file originally posted online, Supplementary Figures 1, 2, 5 and 6 and Supplementary Tables 2–4, 6 and 11 contained errors. Corrected versions of these, as well as two new figures—Supplementary Figures 7 and 8—have been appended to this file as of 27 August 2014. See the article corrigendum for full details.

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Supplementary Information

Genome-wide genetic changes during modern breeding of maize

Yinping Jiao*, Hainan Zhao*, Longhui Ren* Weibin Song*, Biao Zeng, Jinjie Guo, Baobao

Wang, Zhipeng Liu, Jing Chen, Wei Li, Mei Zhang, Shaojun Xie, Jinsheng Lai†

State Key Lab of Agrobiotechnology and National Maize Improvement Center, China

Agricultural University, Beijing 100193, P. R. China

*These authors contributed equally to this work.

†To whom correspondence should be addressed.

E-mail: [email protected]

Nature Genetics: doi:10.1038/ng.2312

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1. Supplementary Tables

Supplementary Table 1. The details of the name and sequencing depth of the 278 inbred lines. Group Name Sequencing depth

Elite Chinese zheng58 28.41

Elite Chinese 178 5.00



Elite Chinese zong31 6.17

Elite Chinese D340 5.75

Elite Chinese yu87-1 6.5

Elite Chinese longkang11 6.22

Elite Chinese luyuan92 2.08

Elite Chinese shen137 2.06

Elite Chinese huangC 2.5

Elite Chinese ye8112 26.37

Elite Chinese zhong451 1.01

Elite Chinese wu125 1.48




Elite Chinese 1205A 2.38

Elite Chinese W499 1.5

Elite Chinese XOP2 1.92


Elite Chinese dan9064 2.15

Elite Chinese R017 1.48

Elite Chinese K10 0.84


Elite Chinese P167 1.25


Elite Chinese M131-5 2.68

Elite Chinese ji444 1.41

Elite Chinese ben7884 1.17


Elite Chinese 4F1 2.35


Elite Chinese hu803 1.34


Elite Chinese cheng698-3 1.97

Elite Chinese su75 0.99

Elite Chinese Beck 1.07



3



Elite Chinese zhonghuang64 1.64

Elite Chinese 698-3 1.9

Elite Chinese DM07 1.59

Elite Chinese changD 1.74

Elite Chinese M101 1.3


Elite Chinese jiutai1 1.55

Elite Chinese hai9-21 1.06



Elite Chinese baihe43 0.79

Elite Chinese jiu138-5 2.14

Elite Chinese ning55 1.29

Elite Chinese han21 1.23

Elite Chinese huotanghuang 1.47

Elite Chinese FC-13 0.99



Elite Chinese huo17 1.25

Elite Chinese ernan24 2.22

Elite Chinese chang7-2 24.95


Elite Chinese danhuang02 6.34

Elite Chinese lv28 2.51


Elite Chinese hai1134 1.86


Elite Chinese huangyesi3 2.38

Elite Chinese wenhuang31413 1.76

Elite Chinese chang72 1.52

Elite Chinese 3H2 1.32

Elite Chinese xun92-8 1.1

Elite Chinese tangsipingtou 1.69



Elite Chinese zi330 0.88

Elite Chinese huangyesi 1.61

Elite Chinese tie7922 1.5



Elite Chinese Maxa 1.03

Elite Chinese wu126 1.66


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Elite Chinese yi36 0.83

Elite Chinese nan21-3 1.45

Elite Chinese shangyin110-1 1.37

Elite Chinese huotanghuang17 2.47

Elite Chinese fu8521 1.11

Elite Chinese DH149 1.23

Elite Chinese guan17-1 0.58


Elite Chinese 807D 0.71



Elite Chinese liao2202 0.5

Elite Chinese niu2-1 0.59


Elite Chinese huangchangb 0.5

Elite Chinese zaC546 1.17

Elite Chinese H21 0.78

Elite Chinese shuang741 0.73

Elite Chinese 200B 1.41

Elite Chinese chong72 0.76

Elite Chinese yu537A 0.85

Elite Chinese dong327 0.87

Elite Chinese N138 1.81

Elite Chinese chengzi108 0.98




Elite Chinese Lx9801 0.76

Elite Chinese E28 0.67

Elite Chinese zhongyin15 1.17

Elite Chinese zong3 0.96




Elite Chinese qi205 0.63


Elite Chinese huangzaosi 8.31


Elite Chinese siyi 0.83

Elite Chinese xun971 0.67

Elite Chinese xinlun5-9 0.57

Elite Chinese fengke1 0.74

Elite Chinese huobai 1.58

Elite Chinese H127 5.41


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Elite Chinese suwan1611 1.91

Elite Chinese xiangai3 2.94

Elite Chinese qiong51 2.44

Elite Chinese xing230 1.63

Elite Chinese Yd6 1.71

Elite Chinese dai6 1.36

Elite Chinese yu374 1.4

Elite Chinese changK 4.13

Elite Chinese tian77 1.09

Elite Chinese lian87 0.82

Elite Chinese L-1 1.03

Elite Chinese bao3040 1.23

Elite Chinese yu82 1.06

Elite Chinese fu8701 0.9

Elite Chinese shan89 1


Elite Chinese fusheA 2.15

Elite Chinese cheng18 2.14

Elite Chinese Q1261 1.89


Elite Chinese jiao05 1.7


Elite Chinese hai014 1.28

Elite Chinese S22 1.21

Elite Chinese lv45 0.84

Public_US B73 5.00

Public_US B95 2.91

Public_US B98 2.62

Public_US B12 2.39

Public_US A632 2.37

Public_US CI66 1.7

Public_US W117 1.67

Public_US CM105 1.54

Public_US IA5125 1.52

Public_US OH43 1.51

Public_US H99 1.46

Public_US B8 1.46

Public_US Mo24W 1.44

Public_US B7 1.37

Public_US NC268 1.29

Public_US W64a 1.23

Public_US M14 1.17

Public_US W153R 1.16

Public_US W182bn 1.13


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Public_US HP301 1.08

Public_US B394 1.05

Public_US A554 0.98

Public_US P39 0.92

Public_US CN165 0.9

Public_US H105W 0.89

Public_US A679 0.88

Public_US Pa91 0.86

Public_US Va26 0.82

Public_US H84 0.75

Public_US W23 0.69

Public_US De811 0.67

Public_US B76 0.66

Public_US B100 0.65

Public_US Sg1533 0.6

Public_US B68 0.59

Public_US Mo17 20.00

Ex-PVP PHN82 2.78

Ex-PVP PHR63 2.77

Ex-PVP IBB15 2.64

Ex-PVP PHZ51 2.57

Ex-PVP PHP55 2.48

Ex-PVP PHM10 2.24

Ex-PVP PHW03 2.22

Ex-PVP 807 2.21

Ex-PVP RS710 2.08

Ex-PVP LH39 2.05

Ex-PVP Q381 2.01

Ex-PVP MBPM 2.01

Ex-PVP LH143 1.97

Ex-PVP PHP85 1.96

Ex-PVP PHW20 1.95

Ex-PVP LH127 1.94

Ex-PVP PHW51 1.83

Ex-PVP MBST 1.8

Ex-PVP LH194 1.79

Ex-PVP PHV37 1.78

Ex-PVP PHJ31 1.76

Ex-PVP LH205 1.75

Ex-PVP LH38 1.74

Ex-PVP 78371A 1.66

Ex-PVP LH57 1.52

Ex-PVP PHW43 1.49

Ex-PVP LH191 1.49


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Ex-PVP PHV78 1.47

Ex-PVP PHG71 1.46

Ex-PVP 207 1.39

Ex-PVP 11430 1.39

Ex-PVP LH149 1.38

Ex-PVP PHG50 1.38

Ex-PVP 6103 1.36

Ex-PVP 794 1.34

Ex-PVP LH52 1.31

Ex-PVP LH54 1.29

Ex-PVP PHW52 1.27

Ex-PVP LH1 1.25

Ex-PVP PHN11 1.21

Ex-PVP PHN47 1.21

Ex-PVP PHT10 1.18

Ex-PVP E8501 1.18

Ex-PVP LH61 1.16

Ex-PVP 78010 1.08

Ex-PVP PHG83 1.08

Ex-PVP LH51 1.06

Ex-PVP LH192 1.06

Ex-PVP PHR32 1.05

Ex-PVP PHJ75 1.05

Ex-PVP 787 1.04

Ex-PVP PHN29 1.02

Ex-PVP CR1HT 0.97

Ex-PVP S8324 0.97

Ex-PVP 4676A 0.96

Ex-PVP PB80 0.95

Ex-PVP 2369 0.94

Ex-PVP IB014 0.91

Ex-PVP IB02 0.89

Ex-PVP WIL903 0.89

Ex-PVP PHJ40 0.89

Ex-PVP NS501 0.87

Ex-PVP CR14 0.87

Ex-PVP NS701 0.86

Ex-PVP H8431 0.85

Ex-PVP LH190 0.84

Ex-PVP 87916W 0.84

Ex-PVP PHG84 0.83

Ex-PVP PHM57 0.79

Ex-PVP PHP60 0.79

Ex-PVP LH93 0.78


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Ex-PVP 2MA22 0.78

Ex-PVP WIL901 0.78

Ex-PVP IBB14 0.75

Ex-PVP B47 0.72

Ex-PVP L135 0.71

Ex-PVP PHH93 0.71

Ex-PVP 790 0.69

Ex-PVP WIL500 0.69

Ex-PVP PHK76 0.68

Ex-PVP BS110 0.68

Ex-PVP PHJ70 0.67

Ex-PVP PHR36 0.66

Ex-PVP PHT60 0.64

Ex-PVP DJ7 0.63

Ex-PVP FAPW 0.6

Ex-PVP PHG35 0.56

Ex-PVP LH202 0.55

Ex-PVP 78002A 0.54

Ex-PVP LH60 0.5


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Supplementary Table 2. SNPs identified from three groups of the 278 inbred lines.

total SNP SNP in gene SNP in coding region

No.of SNP No.of gene No.of SNP No.of gene

Elite Chinese lines 4,492,374 710,534 28,662 175,165 22,634

Public US lines 2,955,927 513,375 27,612 126,372 20,950

Ex-PVP lines 3,460,701 570,328 28,009 142,121 21,426

total 4,750,376 741,823 28,763 183,568 22,809


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Supplementary Table 3. The top five signals of genome-wide significant association of three traits. Trait Chromosome Position -log10p

Silk color 10 138,090,892 5.96 Silk color 10 138,453,309 5.95 Silk color 10 138,453,348 5.95 Silk color 10 138,461,950 6.16 Silk color 10 138,462,086 6.04

Days to anthesis 4 152,721,073 5.85 Days to anthesis 4 152,733,096 5.93 Days to anthesis 4 152,763,319 6.54 Days to anthesis 4 152,788,672 5.82 Days to anthesis 8 130,749,583 5.75

Cob color 1 47,805,826 18.42 Cob color 1 47,806,960 16.71 Cob color 1 47,807,004 16.71 Cob color 1 47,993,467 17.04 Cob color 1 48,024,206 23.97


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Supplementary Table 4. Tajima’s D and nucleotide diversity (π) of the three maize groups. Public US lines Ex-PVP lines Elite Chinese lines

D of whole genome -0.46 -0.33 -0.28

D of genic region -0.08 0.13 0.25

D of seletion targets -1.25 -1.70 -1.54

π of whole genome 0.0056 0.0050 0.0055

π of genic region 0.0051 0.0045 0.0050

π of seletion targets 0.0033 0.0019 0.0018


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Supplementary Table 6. The list of selective target genes with function reported. The highlighted six genes have their function reported in Arabidopsis or rice.

Gene ID Group Annotation GRMZM2G088753 Ex-PVP starch branching enzyme1(sbe1)1 GRMZM2G057116 Ex-PVP WRKY transcription factor 102 GRMZM2G300348 Ex-PVP phytoene synthase (y1)3 GRMZM2G078798 Ex-PVP gibberellin catabolism ga2ox14 GRMZM2G132898 Ex-PVP CTP:phosphorylcholine cytidylyltransferase5 GRMZM2G163242 Ex-PVP Armadillo repeat protein ARO16 GRMZM2G175755 Public US plastid ribosomal protein ZmPRPL35-17 GRMZM2G103881 Public US staygreen protein Sgr8 GRMZM2G123815 Public US grain size 5 GS59 GRMZM2G026939 Public US 19kD alpha zein B110 GRMZM2G123587 Elite Chinese DEMETER11 GRMZM2G420801 Elite Chinese Ethylene receptor12 GRMZM2G121897 Elite Chinese transcription factor subunit NF-YB213 GRMZM5G836729 Elite Chinese PHD finger protein14


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Supplementary Table 7. Summary of deep sequencing of 4 inbred lines.

Total reads Mean depth

Mapped reads Mapped Loci

(bp) Genome Coverage

5003 865,906,052 27.75 767,409,698 1,929,008,764 93.38% 8112 686,951,880 26.37 635,972,244 1,927,832,916 93.32% 478 808,071,846 28.93 752,962,916 1,929,588,103 93.41%

Zheng58 825,818,942 28.41 749,156,526 1,923,145,810 93.10%


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Supplementary Table 8. SNP annotation of 4 deep sequenced inbred lines.

Total snp SNP in gene SNP in coding region Large-effect SNP

No. of SNP

No. of gene

No. of SNP

No. of gene

No. of SNP

No. of gene

8112 1,360,989 287,096 17,345 66,467 10,872 1,435 1,231 5003 2,804,969 581,633 34,337 146,247 26,233 653 555 478 2,357,065 500,009 27,079 129,355 21,609 1,150 979 Zheng58 2,789,175 558,948 30,883 146,640 24,968 1,343 1,171 total 5,058,396 895,527 31,262 216,923 27,042 2,153 1,986


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Supplementary Table 9. 1-10bp insertion and deletion annotation of 4 deep sequenced inbred lines.

Total indel

Gene region Coding region No. of indel No. of gene No. of indel No. of gene

5003 91,264 15,332 8,861 914 837 8112 83,486 10,643 5,755 626 566 478 92,586 14,071 7,663 798 718 Zheng58 97,946 15,320 8,453 855 775 total 287,504 44,305 16,026 2,595 2,037


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Supplementary Table 10. Summary of the validation of the SNP calling of 4 deep sequencing through local De novo assembly.

No.of genes Average No.

of contigs Average length

of contigs No. of

SNPs compared Consistent rate

Zheng58 560 2.6 1,277 8,219 99.30% 5003 504 2.7 1,167 7,580 99.40% 478 576 2.7 1,213 7,980 99.50% 8112 545 2.8 1,155 3,975 99.40%


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Supplementary Table 11. Pattern of copy number variation for CNV genes across breeding. Copy numbers of CNV genes were investigated within a pedigree from 5003 and 8112 to 478. Up CNV, genes with copy number in offspring higher than any parents; down CNV, genes with copy number in offspring lower than any parents, Additive CNV, genes with copy number in offspring between that of their two parents.

Genes with CNV between parents

Genes do not shown CNV between parents

Up CNV 98 298 Additive CNV 2,085 - Down CNV 144 227

Total genes with CNV 2,327 525


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2. Supplementary Figures

Supplementary Figure 1. The GWAS results of silk color and days to anthesis. (a) Manhattan plot of GWAS result for silk color. (b) Quantile-quantile plot of GWAS result for silk color. (c). Regional Manhattan plot of 5Mb around the peak SNP of GWAS result for silk color. (d) Manhattan plot of GWAS result for days to anthesis. (e) Quantile-quantile plot of GWAS result for days to anthesis. (f). Regional Manhattan plot of 5Mb around the peak SNP of GWAS result for days to anthesis.


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Supplementary Figure 2. CLR and genetic diversity of chromosome 2-10 of three maize inbred groups. Green lines represents public US subgroup, blue lines the Ex-PVP subgroup and dark red lines the Chinese group. Orange lines represents FST of China and US (both public US lines and Ex-PVP lines) maize group, Purple lines represents FST of public US group and Ex-PVP group. CLR and genetic diversity of chromosome 2.


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Supplementary Figure 2. CLR and genetic diversity of chromosome 2-10 of three maize inbred groups (continue). CLR and genetic diversity of chromosome 3.


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Supplementary Figure 3. Pedigree of 4 deep sequenced lines.


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Supplementary Figure 4. The length distribution of the 1-10bp indels from 4 deep sequenced inbred lines.


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Supplementary Figure 5. The mutation rate of transition and transversion.


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Supplementary Figure 6. The distribution of allele frequency of SNPs associated with important agronomic traits. These trait-associated SNPs are all from the GWAS studies of NAM population.


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Supplementary Figure 7. Genetic distance of inbred lines related to B73 and Mo17. A, Genetic distance between six lines (DJ7, LH202, LH149, PB80, LH194 and LH192) and B73. B, Genetic distance between seven lines (LH51, LH54, LH52, LH61, LH57, CR1HT and LH60) and Mo17.


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Supplementary Figure 8. Distribution of genetic distance of each 5Mb windows. Red line indicates genetic distance of 0.05.


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References

1. Xia, H., Yandeau-Nelson, M., Thompson, D.B. & Guiltinan, M.J. Deficiency of maize starch-branching enzyme I results in altered starch fine structure, decreased digestibility and reduced coleoptile growth during germination. BMC Plant Biol 11, 95 (2011). 2. Zhang, Z.L. et al. A rice WRKY gene encodes a transcriptional repressor of the gibberellin signaling pathway in aleurone cells. Plant Physiol 134, 1500-13 (2004). 3. Buckner, B., Miguel, P.S., Janick-Buckner, D. & Bennetzen, J.L. The y1 gene of maize codes for phytoene synthase. Genetics 143, 479-88 (1996). 4. Bolduc, N. & Hake, S. The maize transcription factor KNOTTED1 directly regulates the gibberellin catabolism gene ga2ox1. Plant Cell 21, 1647-58 (2009). 5. Inatsugi, R., Nakamura, M. & Nishida, I. Phosphatidylcholine biosynthesis at low temperature: differential expression of CTP:phosphorylcholine cytidylyltransferase isogenes in Arabidopsis thaliana. Plant Cell Physiol 43, 1342-50 (2002). 6. Gebert, M., Dresselhaus, T. & Sprunck, S. F-actin organization and pollen tube tip growth in Arabidopsis are dependent on the gametophyte-specific Armadillo repeat protein ARO1. Plant Cell 20, 2798-814 (2008). 7. Magnard, J.L. et al. Morphogenesis of maize embryos requires ZmPRPL35-1 encoding a plastid ribosomal protein. Plant Physiol 134, 649-63 (2004). 8. Park, S.Y. et al. The senescence-induced staygreen protein regulates chlorophyll degradation. Plant Cell 19, 1649-64 (2007). 9. Li, Y. et al. Natural variation in GS5 plays an important role in regulating grain size and yield in rice. Nat Genet 43, 1266-9 (2011). 10. Woo, Y.M., Hu, D.W., Larkins, B.A. & Jung, R. Genomics analysis of genes expressed in maize endosperm identifies novel seed proteins and clarifies patterns of zein gene expression. Plant Cell 13, 2297-317 (2001). 11. Choi, Y. et al. DEMETER, a DNA glycosylase domain protein, is required for endosperm gene imprinting and seed viability in arabidopsis. Cell 110, 33-42 (2002). 12. Gallie, D.R. & Young, T.E. The ethylene biosynthetic and perception machinery is differentially expressed during endosperm and embryo development in maize. Mol Genet Genomics 271, 267-81 (2004). 13. Nelson, D.E. et al. Plant nuclear factor Y (NF-Y) B subunits confer drought tolerance and lead to improved corn yields on water-limited acres. Proc Natl Acad Sci U S A 104, 16450-5 (2007). 14. Sung, S., Schmitz, R.J. & Amasino, R.M. A PHD finger protein involved in both the vernalization and photoperiod pathways in Arabidopsis. Genes Dev 20, 3244-8 (2006).


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Genome-wide genetic changes during modern breeding of maize · 2017-03-13 · Elite Chinese chang7-2 24.95 Elite Chinese dan340 7.05 Elite Chinese danhuang02 6.34 Elite Chinese lv28