Danforth 2015
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This document summarizes research on adaptation in maize during and after domestication. It discusses how maize adapted through standing genetic variation, regulatory changes, and polygenic adaptation using multiple mutations and alleles from teosinte. It describes the origins and spread of maize from its ancestor teosinte in Mexico around 9,000 years ago to other regions of Mexico, South America, and beyond. The differences between lowland and highland maize populations are also summarized.
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Danforth 2015
- 1. Adaptation in maize: domestication and beyond Jeffrey Ross-Ibarra @jrossibarra • www.rilab.org Dept. Plant Sciences • Center for Population Biology • Genome Center University of California Davis photo by lady_lbrty
- 2. Brandon Gaut Hocholdinger & Hoecker 2007 TIP Genetics
- 8. hard sweep multiple mutations polygenic adaptation Diversity standing variation “soft” sweeps
- 9. M T G P H R L GGTCGAC ATG ACT GGT CCA CAT CGA CTG TAG
- 10. 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
- 11. 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
- 12. maize origins TripsacumF1 teosinte (Z. mays ssp. parviglumis) maize (Z. mays ssp. mays)
- 13. F1 Beadle 1979 Field Museum of Nat. Hist. Bull.
- 14. F1 Beadle 1979 Field Museum of Nat. Hist. Bull.
- 15. F1 Beadle 1979 Field Museum of Nat. Hist. Bull.
- 16. F1 Beadle 1979 Field Museum of Nat. Hist. Bull.
- 17. Briggs et al. 2007 Genetics 1 2 3 4 5 6 7 8 9 10
- 18. 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 e internode (in) and glume (gl) labeled. c. Teosinte ear from a plant with a m introgressed into it. d. Close-up of a single teosinte fruitcase. e. Close-up o teosinte plant with a maize allele of tga1 introgressed into it. f. Ear of maiz (Tga1-maize allele) with the cob exposed showing the small white glumes a of maize inbred W22:tga1 which carries the teosinte allele, showing enlarge h. Ear of maize inbred W22 carrying the tga1-ems1 allele, showing enlarged g NIH-PAAuthorManuscriptNIH-PAAuthorManuscriptNIH-P tga1
- 19. 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 e internode (in) and glume (gl) labeled. c. Teosinte ear from a plant with a m introgressed into it. d. Close-up of a single teosinte fruitcase. e. Close-up o teosinte plant with a maize allele of tga1 introgressed into it. f. Ear of maiz (Tga1-maize allele) with the cob exposed showing the small white glumes a of maize inbred W22:tga1 which carries the teosinte allele, showing enlarge h. Ear of maize inbred W22 carrying the tga1-ems1 allele, showing enlarged g NIH-PAAuthorManuscriptNIH-PAAuthorManuscriptNIH-P tga1
- 20. 1 2 3 4 5 6 7 8 9 10 gt1 tga1 Wills et al. 2013 PLoS Genetics
- 21. 1 2 3 4 5 6 7 8 9 10 gt1 tga1 Wills et al. 2013 PLoS Genetics teosinte maize Clint Whipple, BYU
- 22. 1 2 3 4 5 6 7 8 9 10 gt1 tga1 Wills et al. 2013 PLoS Genetics 5’ control region 3’ UTR
- 23. 1 2 3 4 5 6 7 8 9 10 tb1 Studer et al. 2011 Nat. Gen.; Vann et al. 2015 PeerJ tga1gt1
- 24. 1 2 3 4 5 6 7 8 9 10 tb1 Studer et al. 2011 Nat. Gen.; Vann et al. 2015 PeerJ tga1 GENETICS ADVANCE ONLINE PUBLICATION 3 nguish maize and teosinte. Both the maize and teosinte s for the distal component repressed luciferase expression luc luc luc luc luc luc Hopscotch mpCaMV M-dist T-prox M-prox 0 0.5 1.0 1.5 2.0 ∆M-dist ∆M-prox ProximalcontrolregionDistal Constructs and corresponding normalized luciferase expression nsient assays were performed in maize leaf protoplast. Each is drawn to scale. The construct backbone consists of the romoter from the cauliflower mosaic virus (mpCaMV, gray box), ORF (luc, white box) and the nopaline synthase terminator ). Portions of the proximal and distal components of the gion (hatched boxes) from maize and teosinte were cloned ction sites upstream of the minimal promoter. “ ” denotes on of either the Tourist or Hopscotch element from the maize Horizontal green bars show the normalized mean with s.e.m. onstruct. relative expressionconstruct gt1
- 25. 1 2 3 4 5 6 7 8 9 10 tb1 Figure 2 Map of parviglumis Populations and Hopscotch allele frequency. Map showing the frequency of the Hopscotch allele in populations of parviglumis where we sampled more than 6 individuals. Size of circles reflects number of individuals sampled. The Balsas River is shown, as the Balsas River Basin is believed to be the center of domestication of maize. as our independent trait for phenotyping analyses. SAS code used for analysis is available at http://dx.doi.org/10.6084/m9.figshare.1166630. RESULTS Genotyping for the Hopscotch insertion The genotype at the Hopscotch insertion was confirmed with two PCRs for 837 individuals of the 1,100 screened (Table S1 and Table S2). Among the 247 maize landrace accessions genotyped, all but eight were homozygous for the presence of the insertion Within our parviglumis and mexicana samples we found the Hopscotch insertion segregating in 37 (n = 86) and four (n = 17) populations, respectively, and at highest frequency within populations in the states of Jalisco, Colima, and Michoac´an in central-western Mexico (Fig. 2). Using our Hopscotch genotyping, we calculated diVerentiation between populations (FST) and subspecies (FCT) for populations in which we sampled sixteen or more chromosomes. We found that FCT = 0, and levels of FST among populations within each subspecies (0.22) and among all populations (0.23) (Table 1) are similar to genome-wide estimates from previous studies Pyh¨aj¨arvi, 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 and environmental variables (all Bayes Factors < 1). Studer et al. 2011 Nat. Gen.; Vann et al. 2015 PeerJ tga1 GENETICS ADVANCE ONLINE PUBLICATION 3 nguish maize and teosinte. Both the maize and teosinte s for the distal component repressed luciferase expression luc luc luc luc luc luc Hopscotch mpCaMV M-dist T-prox M-prox 0 0.5 1.0 1.5 2.0 ∆M-dist ∆M-prox ProximalcontrolregionDistal Constructs and corresponding normalized luciferase expression nsient assays were performed in maize leaf protoplast. Each is drawn to scale. The construct backbone consists of the romoter from the cauliflower mosaic virus (mpCaMV, gray box), ORF (luc, white box) and the nopaline synthase terminator ). Portions of the proximal and distal components of the gion (hatched boxes) from maize and teosinte were cloned ction sites upstream of the minimal promoter. “ ” denotes on of either the Tourist or Hopscotch element from the maize Horizontal green bars show the normalized mean with s.e.m. onstruct. relative expressionconstruct gt1
- 26. hard sweep M T N P H R L GGTCGA ATG ACT GAT CCA CAT CGA CTG TAG tga1
- 27. 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
- 28. Vann et al. 2015 PeerJ polygenic adaptation 30% phenotypic variance 0% phenotypic variance
- 29. 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:
- 30. Hufford et al. 2012 Nat. Gen. Chia et al. 2012 Nat. Gen 13 teosinte 23 maize genomes:
- 31. Swanson-Wagner et al. 2012 PNAS E Dom/Imp genes (n=1761) 89 4644 1582 twork edges Maize network edges D GRMZM2G068436 GRMZM2G137947 GRMZM2G375302 Mb Mb s with altered expression or conservation and targets of selection during improvement and/or domestication. (A) Venn diagram ween DE genes, AEC genes, and the genes that occur in genomic regions that have evidence for selective sweeps during maize vement (Dom/Imp genes). (B) Teosinte coexpression networks for three genes (GRMZM2G068436, GRMZM2G137947, and t) Edges that are maintained in maize coexpression networks are shown. Although the differentially expressed gene (red node) is
- 32. Beissinger et al. In Prep nucleotidediversity distance to nearest substitution (cM)
- 33. Beissinger et al. In Prep nucleotidediversity distance to nearest substitution (cM)
- 34. how to adapt: domestication standing variation M T G P H R L GGTAAA ATG ACT GGT CCA CAT CGA CTG TAG polygenic adaptation regulatory variation teosinte maize
- 35. Mexico lowland 9,000 BP Matsuoka et al. 2002; Piperno 2006 Perry et al. 2006; Piperno et al. 2009
- 36. Mexico highland6,000 BP Mexico lowland 9,000 BP Matsuoka et al. 2002; Piperno 2006 Perry et al. 2006; Piperno et al. 2009
- 37. Mexico highland6,000 BP S. America lowland 6,000 BP Mexico lowland 9,000 BP Matsuoka et al. 2002; Piperno 2006 Perry et al. 2006; Piperno et al. 2009
- 38. Mexico highland6,000 BP S. America lowland 6,000 BP S. America Highland 4,000 BP Mexico lowland 9,000 BP Matsuoka et al. 2002; Piperno 2006 Perry et al. 2006; Piperno et al. 2009
- 41. SA MEX SA MEX SA MEX SA MEX SA MEX SA MEX Ear Height Plant Height Tassel Br. Number TW Days to Anthesis SA MEX SA MEX SA MEX SA MEX LowlandHighland
- 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 cluding mexicana, in which Mexican Highland maize is tied wit the West Mexico group as the most ancestral population (Fig. 3B To mitigate the impact of introgression, we used a slight modified approach that excludes both parviglumis and mexican and calculates genetic drift with respect to ancestral frequencie inferred from domesticated maize alone. Because the genet Fig. 1. (A) Map of sampled maize accessions colored by genetic group. (B) First three genetic PCs of all sampled accessions. van Heerwaarden et al. PNAS | January 18, 2011 | vol. 108 | no. 3 | 108 van Heerwaarden et al. 2011 PNAS
- 43. 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 cluding mexicana, in which Mexican Highland maize is tied wit the West Mexico group as the most ancestral population (Fig. 3B To mitigate the impact of introgression, we used a slight modified approach that excludes both parviglumis and mexican and calculates genetic drift with respect to ancestral frequencie inferred from domesticated maize alone. Because the genet Fig. 1. (A) Map of sampled maize accessions colored by genetic group. (B) First three genetic PCs of all sampled accessions. van Heerwaarden et al. PNAS | January 18, 2011 | vol. 108 | no. 3 | 108 van Heerwaarden et al. 2011 PNAS
- 44. 95 samples ~100K SNPs Takuno et al. 2015 Genetics
- 45. -Logp-valueFstS.America -Log p-value Fst Mexico shared SNPs unique S.America unique Mexico 95 samples ~100K SNPs Takuno et al. 2015 Genetics
- 46. -Logp-valueFstS.America -Log p-value Fst Mexico shared SNPs unique S.America unique Mexico 39% 61% Intergenic Genic 19% 81% Standing Variation New mutation Takuno et al. 2015 Genetics
- 47. Beissinger et al. In Prep Berg & Coop 2014 PLoS Genetics
- 48. Beissinger et al. In Prep Berg & Coop 2014 PLoS Genetics Z = LX i=1 ↵ipi allele freq.population breeding value effect size
- 49. Beissinger et al. In Prep Berg & Coop 2014 PLoS Genetics Z = LX i=1 ↵ipi allele freq.population breeding value effect size relatednessdispersion add. genetic var. QX = ~Z0 T F 1 ~Z0 2VA
- 50. Beissinger et al. In Prep Berg & Coop 2014 PLoS Genetics Warm
- 51. Cold Beissinger et al. In Prep Berg & Coop 2014 PLoS Genetics Warm
- 52. Cold Beissinger et al. In Prep Berg & Coop 2014 PLoS Genetics Warm
- 53. domesticationhow to adapt: ——————————- standing variation M T G P H R L GGTAAA ATG ACT GGT CCA CAT CGA CTG TAG polygenic adaptation regulatory variation local adaptation
- 55. new mutation
- 56. gene flow new mutation
- 57. Piperno 2006; Perry et al. 2006; Piperno et al. 2009 Mexico highland6,000 BP domestication in Mexico lowland 9,000 BP Photo by Pesach Lubinsky mexicanamaize
- 58. mexicana parviglumis Lauter et al. (2004) Genetics Lowland Photos: Ruairidh Sawers, LANGEBIO Highland maizeteosinte
- 59. mexicana maize references Hufford et al. 2013 PLoS Genetics 0 1000 2000 3000 4000 5000 generations 0 1000 2000 3000 4000 5000 -292000-290000 Nabogame Likelihoods generations comp.loglikelihood 0 1000 2000 3000 4000 5000 -293000-291500-290000 Santa Clara Likelihoods generations comp.loglikelihood 0 100 - 0 100 -296500-294500 Tenang comp.loglikelihood 0 100 -286000-284000 Pur comp.loglikelihood mexicana into maize 0 1000 2000 3000 4000 5000 -412 generations 0 1000 2000 3000 4000 5000 -447000-444000 Nabogame Likelihoods generations comp.loglikelihood 0 1000 2000 3000 4000 5000 -452000-450000 Santa Clara Likelihoods generations comp.loglikelihood 0 1000 2000 3000 4000 5000 -4 generations 0 1000 2000 3000 4000 5000 -406500-404500 Tenango del Aire Likelihoods generations comp.loglikelihood 0 1000 2000 3000 4000 5000 -420000-418500 Puruandiro Likelihoods generations comp.loglikelihood 0 1000 2000 300 - generation 0 1000 2000 300 -418000-416000-414000 Xochimilco Like generation comp.loglikelihood 0 1000 2000 300 -418000-416500 Opopeo Likeli generation comp.loglikelihood 00 San Pedro Likelihoods ihood 0 El Porvenir Likelihoods ihood 10000 Ixtlan Likelih ihood B maize into mexicana years BPyears BP
- 60. El Porvenir Opopeo Xochimilco Puruandiro Tenango del Aire Ixtlan Nabogame Santa Clara San Pedro Allopatric El Porvenir Opopeo Xochimilco Puruandiro Tenango del Aire Ixtlan Nabogame Santa Clara San Pedro Allopatric Hufford et al. 2013 PLoS Genetics
- 61. El Porvenir Opopeo Xochimilco Puruandiro Tenango del Aire Ixtlan Nabogame Santa Clara San Pedro Allopatric Inv4n El Porvenir Opopeo Xochimilco Puruandiro Tenango del Aire Ixtlan Nabogame Santa Clara San Pedro Allopatric Hufford et al. 2013 PLoS Genetics
- 62. El Porvenir Opopeo Xochimilco Puruandiro Tenango del Aire Ixtlan Nabogame Santa Clara San Pedro Allopatric Inv4n El Porvenir Opopeo Xochimilco Puruandiro Tenango del Aire Ixtlan Nabogame Santa Clara San Pedro Allopatric Hufford et al. 2013 PLoS Genetics
- 63. Introgression No Introgression Hufford et al. 2013 PLoS Genetics
- 64. Lauter et al. 2004 Genetics Hufford et al. 2013 PLoS Genetics
- 65. Lauter et al. 2004 Genetics Inv4n b1 Moose et al. 2004 Genetics photobyEdCoe mhl1 Hufford et al. 2013 PLoS Genetics
- 66. Lauter et al. 2004 Genetics Inv4n b1 Moose et al. 2004 Genetics photobyEdCoe mhl1 Hufford et al. 2013 PLoS Genetics 0 50 100 150 200 250 300 0.00.6 Chromosome 1 bp proportionofpopulations 0 0.00.6 proportionofpopulations Mb B gt1 tb1bif2 resistance
- 71. Sattah et al. 2011 PLoS Gen. Williamson et al. 2014 PLoS Gen Hernandez et al. 2011 Science
- 72. Sattah et al. 2011 PLoS Gen. Williamson et al. 2014 PLoS Gen Hernandez et al. 2011 Science
- 73. Sattah et al. 2011 PLoS Gen. Williamson et al. 2014 PLoS Gen Hernandez et al. 2011 Science distance to nearest substitution (cM) scaleddiversity
- 74. • Ne diploids • µ beneficial mutations rate per haploid genome • selection from standing variation when 2Neµ < 1 Messer and Petrov 2013 TIG
- 75. Sattah et al. 2011 PLoS Gen. Williamson et al. 2014 PLoS Gen Hernandez et al. 2011 Science distance to nearest substitution (cM) scaleddiversity 2Neµ > 1 2Neµ < 1
- 76. Sattah et al. 2011 PLoS Gen. Williamson et al. 2014 PLoS Gen Hernandez et al. 2011 Science distance to nearest substitution (cM) scaleddiversity Ne ~ 150,000 Ne ~ 10,000* Ne ~ 2,000,000 Ne ~ 600,000 2Neµ > 1 2Neµ < 1
- 77. M T G P H R L ATG ACT GGT CCA CAT CGA CTG TAG
- 78. M T G P H R L ATG ACT GGT CCA CAT CGA CTG TAG M T N P H R L ATG ACT GAT CCA CAT CGA CTG TAG
- 79. M T G P H R L ATG ACT GGT CCA CAT CGA CTG TAG M T N P H R L ATG ACT GAT CCA CAT CGA CTG TAG
- 80. M T G P H R L ATG ACT GGT CCA CAT CGA CTG TAG M T N P H R L ATG ACT GAT CCA CAT CGA CTG TAG x x x
- 81. M T G P H R L ATG ACT GGT CCA CAT CGA CTG TAG M T N P H R L ATG ACT GAT CCA CAT CGA CTG TAG x xx x
- 82. M T G P H R L ATG ACT GGT CCA CAT CGA CTG TAG M T N P H R L ATG ACT GAT CCA CAT CGA CTG TAG x xx x
- 83. Sattah et al. 2011 PLoS Gen. Williamson et al. 2014 PLoS Gen Hernandez et al. 2011 Science distance to nearest substitution (cM) scaleddiversity Ne ~ 150,000 Ne ~ 10,000* Ne ~ 2,000,000 Ne ~ 600,000 2Neµ > 1 2Neµ < 1
- 84. Sattah et al. 2011 PLoS Gen. Williamson et al. 2014 PLoS Gen Hernandez et al. 2011 Science distance to nearest substitution (cM) scaleddiversity Ne ~ 150,000 Ne ~ 10,000* Ne ~ 2,000,000 Ne ~ 600,000 µ ∝ 130 x 106bp µ ∝ 220 x 106bp µ ∝ 2,500 x 106bp µ ∝ 3,100 x 106bp 2Neµ > 1 2Neµ < 1
- 85. Brandon Gaut maizeArabidopsis Kew C-Value Database log 1C genome size
- 86. Bilinski et al. In Prep 2.50 2.75 3.00 3.25 3.50 3.75 MH ML SAH SAL mexicana parviglumis1CGenomeSize(Gb) Altitude highland lowland 2.50 2.75 3.00 3.25 3.50 3.75 MH ML SAH SAL mexicana parviglumis 1CGenomeSize(Gb) Altitude highland lowland
- 87. Bilinski et al. In Prep
- 88. Bilinski et al. In Prep
- 89. Bilinski et al. In Prep knob 350 (Tr1) knob 180
- 90. Bilinski et al. In Prep
- 91. altitude kinship errorrepeat abundance Bilinski et al. In Prep
- 92. altitude kinship errorrepeat abundance Bilinski et al. In Prep knob 180 knob 350 32 TE families overall TE content total genome size
- 93. altitude kinship errorrepeat abundance genome size Bilinski et al. In Prep knob 180 knob 350 32 TE families overall TE content total genome size
- 94. altitude kinship errorrepeat abundance genome size Bilinski et al. In Prep total genome size
- 95. Rayburn et al. 1994 Plant Breeding Francis et al. 2008. Ann. Bot. excluded. Indeed, if we ignore the marked dis of the y-axis caused by their inclusion, then the n effect is strong for all species regardless of phyl test the rigour of these hypotheses would requi plug the gap between Trillium grandiflorum majority of C-value/cell cycle times analysed he Separate plots for diploids and polyploids show nucleotypic effect on CCT in diploids (Fig. 3; Removing the five diploid outliers (.25 pg) re slope (b ¼ 0.27) by approximately four-fold regression continued to be significant (P , 0. the polyploids, a nucleotypic effect on CCT detected (Fig. 3; Table 2); however, removing the ploid outliers rendered the regression non-signifi 0.03x 2 13.5). This confirms previous work in slope/rate of increase in CCT with increasing higher in diploids than in autopolyploids (Eva 1972). With the exception of Scilla sibirica, CC FIG. 3. DNA C-value (pg) and cell cycle time (h) in the roo istem of a range of diploid and polyploid angiosperms. See regression analyses. 2. DNA C-value (pg) and cell cycle time (h) in the root apical mer- m of a range of (A) eudicots and monocots (n ¼ 110), and (B) eudicots (n ¼ 60). See Table 2 for regression analyses. LE 2. Regression analyses of all data presented in s. 2–4 together with the percentage variance accounted by the regression (R2 ), the level of probability (P) for each regression Francis et al. 2008.Ann. Bot. 0 10 20 30 100 105 110 DNA plants cycle 0 6 late flowering early flowering
- 96. • “Soft sweeps” and polygenic selection predominate in maize • Gene flow may provide a novel source of adaptive alleles • Both population size and mutational target contribute • Large, complex genomes may mean more targets and more soft sweeps in plants • Genome size itself may be adaptive Concluding Thoughts
- 97. Acknowledgments Maize Diversity Group Peter Bradbury Ed Buckler John Doebley Theresa Fulton Sherry Flint-Garcia Jim Holland Sharon Mitchell Qi Sun Doreen Ware Collaborators Jim Birchler Jeremy Berg Graham Coop Nathan Springer Lab Alumni Tim Beissinger (USDA-ARS, Mizzou) Matt Hufford (Iowa State) Tanja Pyhäjärvi (Oulu) Shohei Takuno (Sokendai) Joost van Heerwaarden (Wageningen)