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Ecogen2013
- 1. Evolutionary genetics of adaptation to high altitude in Zea mays Jeff Ross-Ibarra www.rilab.org @jrossibarra
- 2. Acknowledgements R-I Lab Collaborators Ed Buckler (USDA/Cornell) Norm Ellstrand (UC Riverside)
- 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. How do plants adapt to new environments? Clausen, Keck, Heisey
- 5. What is the geneRc basis of adaptaRon? Lowry & Willis 2010 PLoS Biology
- 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. Does parallel phenotype = parallel genotype? Colosimo et al. 2005 Science Kovach et al. 2009 PNAS
- 8. • Highland adapta-on in teosinte • AdapRve introgression in highland maize • Parallel adaptaRon in highland maize • Future direcRons
- 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. mexicana and parviglumis in Mexico masl Bradburd et al. Evolution 2013 Hufford et al. (2012) PLoS ONE
- 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. Figures teosinte populaRon sampling • 20 populaRons, 250 plants • Genotyped at 40,000 SNPs Pyhäjärvi et al. Genome Biology Evolu-on 2013
- 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. GWAS, frequency distribuRons idenRfy candidate SNPs Combined GWAS for temperature/altitude Inv1n Inv9d allele freq. differentiation Hierarchical Fst Outlier heterozygosity
- 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. Candidate SNPs enriched in regulatory regions regulatory <-‐-‐-‐-‐-‐> coding enrichment Climate Hancock et al. 2011 Science Fraser 2013 Genome Research Alelle Freq. Morphology (maize)
- 17. • Highland adaptaRon in teosinte • Adap-ve introgression in highland maize • Parallel adaptaRon in highland maize • Future direcRons
- 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. 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. 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. 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. 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. 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. 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. 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. IdenRfying admixture along the genome Chromosome 4: maize (STRUCTURE) 0 50 100 150 200 250
- 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. 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. 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. Shared introgression from teosinte into maize El Porvenir Opopeo Santa Clara Nabogame Puruandiro Xochimilco Tenango del Aire San Pedro Ixtlan Allopatric
- 31. Shared introgression from teosinte into maize El Porvenir Opopeo Santa Clara Nabogame Puruandiro Xochimilco Tenango del Aire San Pedro Ixtlan Allopatric Inv4n
- 32. Shared introgression from teosinte into maize El Porvenir Opopeo Santa Clara Nabogame Puruandiro Xochimilco Tenango del Aire San Pedro Ixtlan Allopatric Inv4n
- 33. Shared introgression from teosinte into maize El Porvenir Opopeo Santa Clara Nabogame Puruandiro Xochimilco Tenango del Aire San Pedro Ixtlan Allopatric Inv4n
- 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. 6 of 9 introgressions overlap with teosinte QTL Inv4n Moose et al. 2004 Genetics b1 in maize Lauter et al. 2004 Genetics
- 36. Introgressed pops show highland phenotypes, cold adaptaRon Introgression No Introgression
- 37. • Highland adaptaRon in teosinte • AdapRve introgression in highland maize • Parallel adapta-on in highland maize • Future direcRons
- 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. 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. 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. 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. 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. Mexican/Andean maize data • 96 samples from four highland/lowland populaRons • 100K SNPS (GBS & Maize SNP50 array) Shohei Takuno
- 44. Modeling demography to idenRfy outliers ! Mexico Using&da/di&for¶meter&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. ! ! Using&da/di& Using&da/di&for¶meter& 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. 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. 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. 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. • Highland adaptaRon in teosinte • AdapRve introgression in highland maize • Parallel adaptaRon in highland maize • Future direc-ons
- 50. Full genomes, new highlands Vince Buffalo MaL Hufford
- 51. Full genomes, new highlands Ne Li & Durbin 2011 Nature Years Vince Buffalo MaL Hufford
- 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. Correlation Coefficient ElevaRon paIerns teosinte-‐mycorrhizae coevoluRon Sharon Strauss Anna O’Brien
- 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. 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