JGI: Genome size impacts on plant adaptation
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Genome size may impact how plant genomes adapt, offering larger mutational targets leading to more adaptation from standing variation and more adaptation in noncoding regions.
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JGI: Genome size impacts on plant adaptation
- 1. Adaptation in plant genomes: a role for genome size? 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. Kew C-Value Database Gaut and Ross-Ibarra 2008 Paris Japonica 150GB Genome Genlisia aurea 63MB Genome Michal Rubeš wide variation in genome size in plants
- 3. Kew C-Value Database what explains genome size variation? Lynch & Connery 2003 ScienceWhitney et al. 2010 Evolution
- 4. Kew C-Value Database what explains genome size variation? Lynch & Connery 2003 ScienceWhitney et al. 2010 Evolution
- 5. seed weight Knight et al 2005 AoB genome size genomesize leafarea correlates of genome size: phenotypes across species
- 6. elevation genomesize Bilinski et al. In Prep correlates of genome size: altitude within Zea mays 0 10 20 30 100 105 110 DNA plants cycle 0 6 genome size late flowering early flowering Rayburn et al. 1994 Plant Breeding #plants
- 7. hard sweep how do genomes adapt?
- 8. hard sweep how do genomes adapt?
- 9. hard sweep how do genomes adapt?
- 10. hard sweep multiple mutations standing variation “soft” sweeps how do genomes adapt?
- 11. hard sweep multiple mutations polygenic adaptation standing variation “soft” sweeps how do genomes adapt?
- 12. M T G P H R L GGTCGAC ATG ACT GGT CCA CAT CGA CTG TAG
- 13. 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 structural change to protein
- 14. 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 regulatory change to expression
- 15. 1.5 2.5 3.5 4.5 Angiosperm average 6400 Mb Non-TE DNA TE DNA Log(genomesizeinMb) 0 1,500 3,000 4,500 6,000 0 1500 3000 4500 6000 Genomesize(Mb) TE content (Mb) r = 0.99 Arabidopsisthaliana Arabidopsislyrata Brachypodiumdistachyon Papaya Rice Lotusjaponicus Blackcottonwood Grapevine Cabbage Medicagotrunculata Sorghum Soybean Levantcotton Maize Aegilopsspeltoides Barley Thursday, May 6, 2010 Tenaillon et al. 2010 TIP Springer et al. 2016 Plant Cell
- 16. Tenaillon et al. 2010 TIP Springer et al. 2016 Plant Cell
- 17. Ne individuals, µ beneficial mutation rate per trait bigger genome, larger mutation target, higher µ selection from standing variation when 2Neµ > 1 predict that larger genomes adapt via noncoding changes, standing variation
- 18. Hancock et al 2011 Science enrichment? no<———>yes Arabidopsis adaptation predominantly coding intergenic synonymous nonsynonymous
- 19. maize (2.5Gb)Arabidopsis log 1C genome size Suketoshi how does adaptation work in maize?
- 20. maizeteosinte
- 21. standing variation RE GENETICS ADVANCE ONLINE PUBLICATION 3 on rate21, strongly suggesting that the Hopscotch insertion (and he older Tourist as well) existed as standing genetic variation in osinte ancestor of maize. Thus, we conclude that the Hopscotch on likely predated domestication by more than 10,000 years and urist insertion by an even greater amount of time. identified four fixed differences in the portion of the proximal stal components of the control region that show evidence of on. We used transient assays in maize leaf protoplasts to test r differences for effects on gene expression. Maize and teosinte osomal segments for the portions of the proximal and distal onents with these four differences were cloned into reporter ucts upstream of the minimal promoter of the cauliflower c virus (mpCaMV), the firefly luciferase ORF and the nopaline se (NOS) terminator (Fig. 4). Each construct was assayed for escence after transformation by electroporation into maize pro- t. The constructs for the distal component contrast the effects Tourist insertion plus the single fixed nucleotide substitution istinguish maize and teosinte. Both the maize and teosinte ucts for the distal component repressed luciferase expression 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 Teosinte cluster haplotype Maize cluster 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-prox ProximalcontrolregionDistalcontrolregion Relative expression 4 Constructs and corresponding normalized luciferase expression Transient assays were performed in maize leaf protoplast. Each uct is drawn to scale. The construct backbone consists of the al promoter from the cauliflower mosaic virus (mpCaMV, gray box), ase ORF (luc, white box) and the nopaline synthase terminator box). Portions of the proximal and distal components of the region (hatched boxes) from maize and teosinte were cloned striction sites upstream of the minimal promoter. “ ” denotes ision of either the Tourist or Hopscotch element from the maize uct. Horizontal green bars show the normalized mean with s.e.m. h construct. relative expressionconstruct Studer et al. 2011 Nat. Gen.; Vann et al. 2015 PeerJ enhances expression teosinte branched - tb1
- 22. hard sweep Figure 1. Phenotypes. a. Maize ear showing the cob (cb) exposed at top. b. Teosinte ear with the rach internode (in) and glume (gl) labeled. c. Teosinte ear from a plant with a maize allele of tga Wang et al. Page 1 NIH-PAAuthorManuscriptNIH-PAAuthorManuscript Wang et al. 2015 Genetics protein change teosinte glume architecture - tga1
- 23. multiple mutations Wills et al. 2013 PLoS Genetics teosinte maize Clint Whipple, BYU grassy tillers - gt1 5’ control region 3’ UTRmodifies expression
- 24. 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
- 25. Hufford et al. 2012 Nat. Gen. Chia et al. 2012 Nat. Gen 13 teosinte 23 maize genomes: genome-wide evidence of adaptation
- 26. Hufford et al. 2012 Nat. Gen. Chia et al. 2012 Nat. Gen 13 teosinte 23 maize genomes: genome-wide evidence of adaptation
- 27. Hufford et al. 2012 Nat. Gen. Chia et al. 2012 Nat. Gen 13 teosinte 23 maize genomes: 5-10% selected regions do not include genes genome-wide evidence of adaptation
- 28. E D Mb nd targets of selection during improvement and/or domestication. (A) Venn diagram that occur in genomic regions that have evidence for selective sweeps during maize oexpression networks for three genes (GRMZM2G068436, GRMZM2G137947, and pression networks are shown. Although the differentially expressed gene (red node) is ize. However, some parts of the teosinte network are still conserved in maize. (C) Cross- vidence for a selective sweep that occurs on chromosome 9. The tick marks along the x ZM2G448355) that was chosen as the candidate target of selection and is differentially ExpressionGenealogy teosinte maize • ~500 selected regions • 11M shared vs 3000 fixed SNPs • show differential expression, decreased expression variation selection on regulatory sequence, standing variation Hufford et al. 2012 Nat. Gen. Swanson-Wagner et al. 2012 PNAS
- 29. Beissinger et al. BioRxiv nucleotidediversity distance to nearest substitution (cM) hard sweeps in genes play minor role in maize
- 30. Beissinger et al. BioRxiv nucleotidediversity distance to nearest substitution (cM) hard sweeps in genes play minor role in maize
- 31. Wallace et al. 2014 PLoS Genetics QTL alleles enriched for noncoding Rodgers-Melnick et al. 2016 PNAS Variance PartitioningGWAS candidate SNPs
- 32. Makarevitch et al. 2015 PLoS Genetics
- 33. Makarevitch et al. 2015 PLoS Genetics single TE family many genes
- 34. Makarevitch et al. 2015 PLoS Genetics single TE family many genes w insertions activate expression GRMZM2G071206 stress/control) 2 4 6 8 10 12 -2 0 2 4 6 8 10 12 14 Lines with the TE insertion Lines without the TE insertion GRMZM2G108149 A B Log2(stress/control) httpDownloaded from Oh43 B73 Mo17 alaw dagaf etug flip gyma ipiki jeli joemon naiba nihep odoj pebi raider riiryl ubel uwum Zm00346 Zm02117 Zm03238 Zm05382 Salt UV Heat Cold on September 9, 2014http://biorxiv.org/Downloaded from * ** ** * * single gene, many individuals
- 35. how to adapt: Zea mays M T G P H R L GGTAAA ATG ACT GGT CCA CAT CGA CTG TAG regulatory variation (including TEs) multiple mutations “soft” sweeps standing variation
- 36. Sattah et al. 2011 PLoS Gen. Williamson et al. 2014 PLoS Gen Hernandez et al. 2011 ScienceRoss-Ibarra et al. 2009 Genetics
- 37. Sattah et al. 2011 PLoS Gen. Williamson et al. 2014 PLoS Gen Hernandez et al. 2011 ScienceRoss-Ibarra et al. 2009 Genetics
- 38. Sattah et al. 2011 PLoS Gen. Williamson et al. 2014 PLoS Gen Hernandez et al. 2011 Science diversity distance from substitution Ross-Ibarra et al. 2009 Genetics
- 39. Sattah et al. 2011 PLoS Gen. Williamson et al. 2014 PLoS Gen Hernandez et al. 2011 Science diversity distance from substitution 20% nonsyn. adaptive 10% nonsyn. adaptive 50% nonsyn. adaptive 40% nonsyn. adaptive Ross-Ibarra et al. 2009 Genetics
- 40. Ne effective number of diploid individuals s selection coefficient selection is effective if 2Nes > 1 differences in adaptation due to drift and small population size?
- 41. 0.05Na Na Na 3NaNe ~ 450,000 Beissinger et al. BioRxiv
- 42. 0.05Na Na Na 3NaNe ~ 450,000 Beissinger et al. BioRxiv Ne ~ 1,000,000
- 43. 0.05Na Na Na 3NaNe ~ 450,000 Beissinger et al. BioRxiv Ne ~ 1,000,000 1e+05 1e+07 1e+09 1e+03 1e+042e+04 1e+05 years(u=3e−8, generation=1) effectivepopulationsize pop BKN_4Hap BKN_6Hap TIL_4Hap_Jalisco TIL_6Hap Ne ~ 1,000,000,000
- 44. 0.05Na Na Na 3NaNe ~ 450,000 Beissinger et al. BioRxiv Ne ~ 1,000,000 1e+05 1e+07 1e+09 1e+03 1e+042e+04 1e+05 years(u=3e−8, generation=1) effectivepopulationsize pop BKN_4Hap BKN_6Hap TIL_4Hap_Jalisco TIL_6Hap Ne ~ 1,000,000,000 Ne ~ 5,000,000,000
- 45. Sattah et al. 2011 PLoS Gen. Williamson et al. 2014 PLoS Gen Hernandez et al. 2011 Science diversity Ne >> 1,000,000 Ne ~ 10,000* Ne ~ 2,000,000 Ne ~ 600,000
- 46. Sattah et al. 2011 PLoS Gen. Williamson et al. 2014 PLoS Gen Hernandez et al. 2011 Science diversity µ ∝ 2,500 Mbp µ ∝ 3,100 Mbp µ ∝ 130 Mbp µ ∝ 220 Mbp
- 47. Pyhäjärvi et al. GBE 2013 enrichment no<———>yes large genomes enriched in noncoding adaptive variants intergenic synonymous nonsynonymous enrichment intergenic<———>coding Hancock et al 2011 Science Fraser et al. 2013 Gen. Research
- 48. Pyhäjärvi et al. GBE 2013 large genomes enriched in noncoding adaptive variantsenrichment intergenic<———>coding excessadaptiveSNPs Hancock et al 2011 Science Fraser et al. 2013 Gen. Research
- 49. • Adaptation in maize occurs from standing variation and targets regulatory variants • Large genomes may have more targets, more standing variation, and more regulatory adaptation • Efforts to identify functional variation should consider genome size in designing experiments and genotyping Genome Size and Adaptation Kew C-Value Database
- 50. Acknowledgments Maize Diversity Group Peter Bradbury Ed Buckler John Doebley Theresa Fulton Sherry Flint-Garcia Jim Holland Sharon Mitchell Qi Sun Doreen Ware Collaborators CSI Davis Nathan Springer Lab Alumni Tim Beissinger (USDA-ARS, Mizzou) Kate Crosby (Monsanto) Matt Hufford (Iowa State) Tanja Pyhäjärvi (Oulu) Shohei Takuno (Sokendai) Joost van Heerwaarden (Wageningen)