Ecogen2013

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Ecogen2013

  1. 1. Evolutionary genetics of adaptation to high altitude in Zea mays   Jeff Ross-Ibarra www.rilab.org @jrossibarra
  2. 2. Acknowledgements R-I Lab Collaborators Ed  Buckler  (USDA/Cornell)   Norm  Ellstrand  (UC  Riverside)  
  3. 3. Acknowledgements R-I Lab Tanja  Pyhäjärvi   (U.  Oulu) Shohei  Takuno   (Sokendai)   Collaborators Ed  Buckler  (USDA/Cornell)   Norm  Ellstrand  (UC  Riverside)   MaIhew  Hufford   (Iowa  State)
  4. 4. How  do  plants  adapt  to  new  environments? Clausen,  Keck,  Heisey
  5. 5. What  is  the  geneRc  basis  of  adaptaRon? Lowry & Willis 2010 PLoS Biology
  6. 6. Supplementary Figure 1 How  common  is  parallel  adaptaRon? LETTERS LETTERS Jin et al. 2008 Nat. Gen. rice Teqing Wild is a Hop inverted Supplementary Figure 1. The phenotypes of Teqing and wild ri ferences whereas delineate To est teosinte, addition this purp the haplo Rose Andrew >95% of somes. T the initia Studer et al. 2011 Nat. Gen. Figure 1 Teosinte and maize p Figure 1 Teosinte and maize plants. (a) Highly branched teosinte plant. gene flow a b c d a
  7. 7. Does  parallel  phenotype  =  parallel  genotype? Colosimo et al. 2005 Science Kovach et al. 2009 PNAS
  8. 8. • Highland  adapta-on  in  teosinte   • AdapRve  introgression  in  highland  maize   • Parallel  adaptaRon  in  highland  maize   • Future  direcRons
  9. 9. Zea:  teosinte  &  maize Tripsacum dactyloides Zea nicaraguensis Zea luxurians Zea diploperennis Zea perennis Zea mays ssp. huehuetenangensis Zea mays ssp. mexicana Zea mays ssp. parviglumis Zea mays ssp. mays Hufford  et  al.  (2012)  Trends  in  Gene.cs
  10. 10. mexicana  and  parviglumis  in  Mexico masl Bradburd et al. Evolution 2013 Hufford  et  al.  (2012)  PLoS  ONE
  11. 11. PutaRve  highland  adaptaRon  in  mexicana mexicana 40 parviglumis Rodriguez et al. (2006) Maydica 30 count subpsecies parviglumis 20 mexicana 10 0 60 80 100 120 days to pollen Barthakur (1974) Int. J Biomet Lauter et al. (2004) Genetics
  12. 12. Figures teosinte  populaRon  sampling • 20  populaRons,  250  plants   • Genotyped  at  40,000  SNPs Pyhäjärvi  et  al.  Genome  Biology  Evolu-on  2013
  13. 13. 0.4 0.6 0.8 r2=0.34 0.2 Inversion  Frequency Inversion Frequency 1.0 Large  inversions  common  and  show  alRtudinal  clines 0.0 edutitla neewteb pihsnoitaler a sa detneserp snoisrevni eerht fo senilc lanidutitlA 8S erugiF hcihw rof sPNS fo rebmun a sa( ecnatsiD .noisrevni hcae nihtiw ecnatsid epytolpah dna ytisrevid wol niam eht ni epytolpah latsid tsom eht morf epytolpah hcae fo )reffid yeht )C dna m4vnI )B ,n1vIn )A .snoitalupop etacidni sroloC .sixa-y eht ni si puorg epytolpah .d9vnI Inv1n 600 800 1000 1200 1400 1600 Inversion  Frequency Altitude (m) AlRtude Figure S4 LD in chromosome 9 among mexicana populations based on SNPs with minor allele frequency >0.1. LD plot of two inversions on chr. 9 in mexicana Inv9d Inv9d AlRtude Figure S8 Altitudinal clines of three inversions presented as a relationship between altitude and haplotype distance within each inversion. Distance (as a number of SNPs for which they differ) of each haplotype from the most distal haplotype in the t  al.  Gene-cs  2012 Fang  e main low diversity haplotype group is in the y-axis. Colors indicate populations. A) nIv1n, B) Inv4m and C)
  14. 14. GWAS,  frequency  distribuRons  idenRfy  candidate  SNPs Combined GWAS for temperature/altitude Inv1n Inv9d allele freq. differentiation Hierarchical Fst Outlier heterozygosity
  15. 15. Candidate  loci  overlap  QTL  for  pigment  &  macrohairs photo by Ed Coe Inv4n Moose et al. 2004 Genetics b1 in maize Lauter et al. 2004 Genetics mhl1 in maize
  16. 16. Candidate  SNPs  enriched  in  regulatory  regions regulatory  <-­‐-­‐-­‐-­‐-­‐>  coding enrichment Climate Hancock  et  al.  2011  Science   Fraser  2013  Genome  Research   Alelle  Freq. Morphology   (maize)
  17. 17. • Highland  adaptaRon  in  teosinte   • Adap-ve  introgression  in  highland  maize   • Parallel  adaptaRon  in  highland  maize   • Future  direcRons
  18. 18. Maize  colonizaRon  of  highlands domestication in Mexico lowland 9,000 BP Matsuoka et al. 2002; Piperno 2006; Perry et al. 2006; Piperno et al. 2009; van Heerwaarden et al. 2011;
  19. 19. Maize  colonizaRon  of  highlands 6,000 BP Mexico highland domestication in Mexico lowland 9,000 BP maize Photo  by  Pesach  Lubinsky Matsuoka et al. 2002; Piperno 2006; Perry et al. 2006; Piperno et al. 2009; van Heerwaarden et al. 2011; mexicana
  20. 20. Parallel  phenotypes  and  admixture  with  teosinte mexicana parviglumis Highland Lowland Photos: Ruairidh Sawers, LANGEBIO Lauter et al. (2004) Genetics                                           2500 2000 m 1500 1000 500 0 mexicana parviglumis South/Caribbean West Highland van  Heerwaarden  et  al.  2011  PNAS
  21. 21. maize  &  teosinte  sympatric  populaRon  sampling Ixtlan Puruandiro El  Porvenir Santa  Clara Xochimilco Opopeo Tenango  del  Aire San  Pedro Amatlan Nabogame Sample:   ✦ ✦ ✦ ✦ ✦ 9  sympatric  populaRon  pairs   2  allopatric  references   120  mexicana   95  maize   40,000  SNPs   Hufford  et  al.  2013  PLoS  Gene-cs
  22. 22. K=7 K=8 K=9 K = 10 K=2 K=3 K=4 K=5 K=6 K=7 K=8 K=9 K = 10 Gene  flow  asymmetric,  mostly  ancient mexicana maize references
  23. 23. Gene  flow  asymmetric,  mostly  ancient mexicana K=2 K=3 K=4 K=5 K=6 K=7 K=8 K=9 K = 10 maize references
  24. 24. Gene  flow  asymmetric,  mostly  ancient mexicana K=2 K=3 K=4 K=5 K=6 K=7 K=8 K=9 K = 10 maize references
  25. 25. 0 San Pedro Likelihoods 1000 2000 3000 4000 -411 c -4125 c B 5000 0 El Porvenir Likelihoods 1000 K=9 4000 0 1000 2000 3000 4000 5000 generations 1000 2000 3000 4000 1000 2000 3000 4000 5000 generations 1000 2000 3000 4000 -288000 -290000 -404500 3000 4000 5000 Tenango del Aire Likelihoods 1000 2000 3000 4000 5000 generations Puruandiro Likelihoods 0 1000 2000 3000 4000 5000 generations Puruandiro Likelihoods 0 1000 2000 3000 4000 5000 generations mexicanaPorvenir Likelihoods El into maize San Pedro Likelihoods 0 2000 maize into mexicana 5000 generations 5000 generations 1000 0 Santa Clara Likelihoods 0 -406500 5000 Santa Clara Likelihoods 0 -294500 3000 -296500 -418500 2000 4000 Tenango del Aire Likelihoods -420000 1000 generations 0 K = 10 comp. log likelihood comp. log likelihood -254000 -444000 -255500 -447000 Nabogame Likelihoods 0 3000 generations -288000 -286000 -284000 K=8 generations 5000 -290000 B 5000 0 1000 2000 3000 4000 5000 generations 0 1000 2000 3000 4000 5000 -290000 00 generations Nabogame Likelihoods . log likelihood generations Tenango del Aire Likelihoods -294500 K=7 comp. log likelihood comp. log likelihood K=6 4000 comp. log likelihood comp. log likelihood K=5 3000 . log likelihood K=4 2000 comp. log likelihood comp. log likelihood comp. log likelihood comp. log likelihood K=3 1000 -290000 K=2 0 -292000 references -254000 -293000 -291500 -290000 -452000 -450000 maize Nabogame Likelihoods -255500 mexicana comp. log likelihood comp. log likelihood Gene  flow  asymmetric,  mostly  ancient generations 2000
  26. 26. IdenRfying  admixture  along  the  genome Chromosome  4:  maize  (STRUCTURE) 0 50 100 150 200 250
  27. 27. IdenRfying  admixture  along  the  genome Chromosome  4:  maize  (STRUCTURE) 0 50 100 150 200 250 • STRUCTURE:  Bayesian  assignment  to  k=2  pops  using  admixture  LD
  28. 28. IdenRfying  admixture  along  the  genome Chromosome  4:  maize  (STRUCTURE) 0 50 100 150 200 250 150 200 250 Chromosome  4:  maize  (HapMix) 0 50 100 Mb • STRUCTURE:  Bayesian  assignment  to  k=2  pops  using  admixture  LD • HAPMIX:  HMM  of  chromosomal  ancestry  along  genome
  29. 29. IdenRfying  admixture  along  the  genome Chromosome  4:  maize  (STRUCTURE) 0 50 100 150 200 250 150 200 250 Chromosome  4:  maize  (HapMix) 0 50 100 Mb • STRUCTURE:  Bayesian  assignment  to  k=2  pops  using  admixture  LD • HAPMIX:  HMM  of  chromosomal  ancestry  along  genome • Shared  regions:  long  shared  haplotypes,  low  FST,  many  shared  SNPs
  30. 30. Shared  introgression  from  teosinte  into  maize El Porvenir Opopeo Santa Clara Nabogame Puruandiro Xochimilco Tenango del Aire San Pedro Ixtlan Allopatric
  31. 31. Shared  introgression  from  teosinte  into  maize El Porvenir Opopeo Santa Clara Nabogame Puruandiro Xochimilco Tenango del Aire San Pedro Ixtlan Allopatric Inv4n
  32. 32. Shared  introgression  from  teosinte  into  maize El Porvenir Opopeo Santa Clara Nabogame Puruandiro Xochimilco Tenango del Aire San Pedro Ixtlan Allopatric Inv4n
  33. 33. Shared  introgression  from  teosinte  into  maize El Porvenir Opopeo Santa Clara Nabogame Puruandiro Xochimilco Tenango del Aire San Pedro Ixtlan Allopatric Inv4n
  34. 34. Shared  introgression  from  teosinte  into  maize El Porvenir Opopeo Santa Clara Nabogame Puruandiro Xochimilco Tenango del Aire San Pedro Ixtlan Allopatric Fst high vs. low elevation maize
  35. 35. 6  of  9  introgressions  overlap  with  teosinte  QTL Inv4n Moose et al. 2004 Genetics b1 in maize Lauter et al. 2004 Genetics
  36. 36. Introgressed  pops  show  highland  phenotypes,  cold  adaptaRon Introgression No  Introgression
  37. 37. • Highland  adaptaRon  in  teosinte   • AdapRve  introgression  in  highland  maize   • Parallel  adapta-on  in  highland  maize   • Future  direcRons
  38. 38. Maize  colonizaRon  of  highlands 6,000 BP Mexico highland Mexico lowland 9,000 BP Matsuoka et al. 2002; Piperno 2006; Perry et al. 2006; Piperno et al. 2009; van Heerwaarden et al. 2011;
  39. 39. Maize  colonizaRon  of  highlands 6,000 BP Mexico highland 6,000  BP Mexico lowland 9,000 BP Matsuoka et al. 2002; Piperno 2006; Perry et al. 2006; Piperno et al. 2009; van Heerwaarden et al. 2011; S.  America   lowland
  40. 40. Maize  colonizaRon  of  highlands 6,000 BP Mexico highland 6,000  BP Mexico lowland S.  America   lowland 9,000 BP 4,000  BP S.  America   Highland Matsuoka et al. 2002; Piperno 2006; Perry et al. 2006; Piperno et al. 2009; van Heerwaarden et al. 2011;
  41. 41. differences between lowland and highland maize in terms of heterozygosity and differentiation from parviglumis (Fig. S3). Structure analysis (21) of all Mexican accessions lends support for this magnitude of introgression (Fig. 2). The three subspecies form clearly separated clusters, but evidence of admixture is the West Mexico group as the most ancestral population (Fig. To mitigate the impact of introgression, we used a sli modified approach that excludes both parviglumis and mexi and calculates genetic drift with respect to ancestral freque inferred from domesticated maize alone. Because the ge photo by Matt Hufford photo by Monthon Wachirasettakul Parallel  phenotypic  adaptaRon  to  highlands Mexico Andes Fig. 1. (A) Map of sampled maize accessions colored by genetic group. (B) First three genetic PCs of all sampled accessions. • shared  phenotypes  between  Mexico  and  Andes   PNAS | January 18, 2011 | vol. 108 | no. 3 | van Heerwaarden et al. • geneRc  data  supports  independent  origin   • independent  mutaRons?  adapRve  gene  flow? van  Heerwaarden  et  al.  2011  PNAS
  42. 42. differences between lowland and highland maize in terms of heterozygosity and differentiation from parviglumis (Fig. S3). Structure analysis (21) of all Mexican accessions lends support for this magnitude of introgression (Fig. 2). The three subspecies form clearly separated clusters, but evidence of admixture is the West Mexico group as the most ancestral population (Fig. To mitigate the impact of introgression, we used a sli modified approach that excludes both parviglumis and mexi and calculates genetic drift with respect to ancestral freque inferred from domesticated maize alone. Because the ge photo by Matt Hufford photo by Monthon Wachirasettakul Parallel  phenotypic  adaptaRon  to  highlands Mexico Andes Fig. 1. (A) Map of sampled maize accessions colored by genetic group. (B) First three genetic PCs of all sampled accessions. • shared  phenotypes  between  Mexico  and  Andes   PNAS | January 18, 2011 | vol. 108 | no. 3 | van Heerwaarden et al. • geneRc  data  supports  independent  origin   • independent  mutaRons?  adapRve  gene  flow? van  Heerwaarden  et  al.  2011  PNAS
  43. 43. Mexican/Andean  maize  data • 96  samples  from  four  highland/lowland  populaRons   • 100K  SNPS  (GBS  &  Maize  SNP50  array) Shohei Takuno
  44. 44. Modeling  demography  to  idenRfy  outliers !  Mexico Using&da/di&for&parameter&estimation Mexico Simulation Observation Observed td te NB Simulated highland allele frequency 0.9NA 0.27NA tf=6,000 0.63NA Lowland Highland Lowland ! South&America S. America td te NB Observed Simulated 0.5NA 0.48NA 0.02NA tf=4,000 >2NA Lowland Highland Lowland lowland allele frequency • Demographic  models  fit  with  joint  site  freq.  spectrum  (δa/δi)   • Simulate  to  generate  null  allele  frequency  distribuRon
  45. 45. !  !  Using&da/di& Using&da/di&for&parameter& AdaptaRon  quanRtaRve,  but  not  parallel Mexico Observation Mexico Observation Simulation unique S. America Highland -Log p-value Fst S. America Maize shared SNPs Lowland REPORTS unique Mexico Yi  et  al.  2010  Science South&America Han  Chinese South&America -Log p-value Fst Mexico • Many  SNPs:  adaptaRon  quanRtaRve   • Sharing  in  Mex./teosinte,  not  Mex./S.  America   • • Lowland Lowland 95%  loci  differ,  80%  from  standing  variaRon   No  enrichment  of  shared  genes Tibetan Fig. 1. Two-dimensional unfolded site frequency spectrum for SNPs in Tibetan (x axis) and Han (y population samples. The number of SNPs detected is color-coded according to the logarithmic s plotted on the right. Arrows indicate a pair of intronic SNPs from the EPAS1 gene that show stro elevated derived allele frequencies in the Tibetan sample compared with the Han sample. Table 1. Genes with strongest frequency changes in the Tibetan population. The top 30 PBS v candidate genes within 100 kb of these loci are noted. For FXYD, F indicates Phe; Y, Tyr; D, Gene Description Lowland EPAS1 C1orf124 DISC1 ATP6V1E2 SPP1 PKLR Lowland Endothelial PAS domain protein 1 (HIF-2a) Hypothetical protein LOC83932 Disrupted in schizophrenia 1 Adenosine triphosphatase (ATPase), H+ transporting, lysosomal 31 kD, V1 Secreted phosphoprotein 1 Pyruvate kinase, liver, and RBC
  46. 46. 0.004 truth 2*s/var cline location 0.002 ACTGCTG 0.000 prob of survival 0.006 Theory  predicts  few  geneRc  parallels  for  highlands −1000 −500 0 500 distance (km) Peter Ralph (USC) Ralph and Coop 2010 Genetics 1000 ACTCCTG
  47. 47. 0.004 truth 2*s/var cline location 0.002 ACTGCTG 0.000 prob of survival 0.006 Theory  predicts  few  geneRc  parallels  for  highlands −1000 −500 0 500 1000 ACTGCTG ACTCCTG distance (km) Tmut = 1/ Peter Ralph (USC) Ralph and Coop 2010 Genetics mut = 2µ⇢Asb ⇠2 ⇡ 104 gens
  48. 48. 0.004 truth 2*s/var cline location 0.002 ACTGCTG 0.000 prob of survival 0.006 Theory  predicts  few  geneRc  parallels  for  highlands −1000 −500 0 500 1000 ACTGCTG ACTCCTG distance (km) Tmut = 1/ Peter Ralph (USC) mut p = 2µ⇢Asb ⇠2 ⇡ 104 gens 34 Tmig = (2/N ) exp(R 2sm / ) ⇡ 5 ⇥ 10 Ralph and Coop 2010 Genetics gens
  49. 49. • Highland  adaptaRon  in  teosinte   • AdapRve  introgression  in  highland  maize   • Parallel  adaptaRon  in  highland  maize   • Future  direc-ons
  50. 50. Full  genomes,  new  highlands Vince  Buffalo MaL  Hufford
  51. 51. Full  genomes,  new  highlands Ne Li & Durbin 2011 Nature Years Vince  Buffalo MaL  Hufford
  52. 52. In  progress:  mapping  pops  &  more  genomes M Hufford (ISU), R. Sawers (Langebio) Summer 2013 S. Flint-Garcia (MU) Winter 2012 MX x MX F2 SA x SA F2 Highland Landrace (PT) x B73 BC2 NILs Highland x Lowland Landrace F2 populations
  53. 53. Correlation Coefficient ElevaRon  paIerns  teosinte-­‐mycorrhizae  coevoluRon Sharon Strauss Anna O’Brien
  54. 54. In  progress:  GWAS  on  temperature  phenotypes Root Signals y–1) 4000 20 rature (°C) after 2h of ction of June or the site of Lycopersicon precipitation herry tomato ilting score of e fully turgid tes that they own are mean 10 8 Chilling sensitivity Wilting score 2 1 6 Gitanshu Munjal 4 Japonica temperate Japonica tropical Indica 2 0 Temperate Tropical 0 0 20 40 60 Latitude (°) Fig. 2. Shoot wilting during root Fig. 3. Chilling sensitivity as a function chilling Plant  Height,  Highland  Temperatures for Oryza sativa at 6°C for Zea mays of latitude of origin genotypes of temperate or genotypes of japonica (temperate or tropical ancestry. A wilting score tropical) or indica ancestry. A chilling of ‘3’ designates that shoots sensitivity score of ‘9’ designates that were fully flaccid, whereas ‘0’ all leaves were yellow as a result of designates fully turgid. Shown water stress at root temperatures are mean ± SE for 8 and 13 below 13°C, whereas ‘1’ designates genotypes of temperate and that none were. Data for yellowing tropical ancestry, respectively. from Mackill & Lei (1997) and data for (unpublished) latitude from Zhao et al. (2011). der rhizosphere chilling, which is associated with wilting (Cruz et al. 2013), Sofiane Mezmouk Arnold Bloom
  55. 55. Conclusions • Parallel  phenotypic  adaptaRon  of  Zea  to  highlands     • Important  roles  for  inversions,  regulatory  mutaRons   • AdaptaRon  to  high  alRtude  quanRtaRve   • Parallel  geneRcs  in  highland  Mexico  via  adapRve  gene  flow   • Different  geneRcs  in  S.  America,  likely  from  standing  variaRon

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