Adaptation in plant genomes: bigger is different

1. Jeffrey Ross-Ibarra @jrossibarra • www.rilab.org Plant Sciences • Center for Population Biology • Genome Center University of California Davis Bigger is different: the role of plant genome size in adaptation

2. Brandon Gaut log haploid genome size Zea maysA. thaliana #species

3. Brandon Gaut log haploid genome size Zea maysA. thaliana #species Springer et al. (2016) Plant Cell 1 Megabase DNA maize Arabidopsis

4. Lloyd et al. 2017 bioRxiv A .thaliana functional prediction

5. Lloyd et al. 2017 bioRxiv A .thaliana functional prediction

6. Lloyd et al. 2017 bioRxiv A .thaliana functional prediction Rodgers-Melnick et al. 2016 PNAS b Ames Diversity Panel Intergenic Open Chromatin (33%) Coding (41%) UTR, proximal % VA explained in maize (height, ﬂowering, etc.)

7. ● ● ● ● 0 5 10 15 20 25 200 400 600 800 1000 Genome Size (Mb) OpenChromatinSize(Mb) Genome_feature ● Exon Intergenic Proximal Total_open_chromatin A 75% 80% 85% 90% 95% %Non−exonicOpenChromatin B Maher et al. 2017 bioRxiv Mei et al. 2017 bioRxiv Rodgers-Melnick et al. 2016 PNAS b Ames Diversity Panel Intergenic Open Chromatin (33%) Coding (41%) UTR, proximal % VA explained in maize (height, ﬂowering, etc.)

8. 25% 75% 78% 22% 0% 25% 50% 75% 100% Arabidopsis Maize Species Percentage Genic Non−genic a 0.0 0.2 0.4 0.6 0.8 100 101 102 103 104 105 106 Arabidopsis non−genic GWAS hits distance to nearest gene (bp, log scale) Density b 0.0 0.2 0.4 0.6 0.8 100 101 102 103 104 105 106 Maize non−genic GWAS hits distance to nearest gene (bp, log scale) Density c Mei et al. 2017 bioRxiv GWAS hits

9. 25% 75% 78% 22% 0% 25% 50% 75% 100% Arabidopsis Maize Species Percentage Genic Non−genic a 0.0 0.2 0.4 0.6 0.8 100 101 102 103 104 105 106 Arabidopsis non−genic GWAS hits distance to nearest gene (bp, log scale) Density b 0.0 0.2 0.4 0.6 0.8 100 101 102 103 104 105 106 Maize non−genic GWAS hits distance to nearest gene (bp, log scale) Density c Mei et al. 2017 bioRxiv GWAS hits

10. Doebley 2004, Studer et al. 2011 tb1 Hopscotch ZmCCT CACTA Yang et al. 2013 plant architecture ﬂowering time

11. Pyhäjärvi et al. 2013 GBEFigure S4 LD in chromosome 9 among mexicana populations based on SNPs with minor allele frequency >0.1. Inv9d Inv9e

12. Inv4n macrohairs, anthocyanin Hufford et al. 2013 PLoS Genetics Pyhäjärvi et al. 2013 GBEFigure S4 LD in chromosome 9 among mexicana populations based on SNPs with minor allele frequency >0.1. Inv9d Inv9e Pyhäjärvi et al. 2013 GBE

13. 4% of B73 absent ~8% absent 30% of the low copy sequence absent from reference genome %readsunmappedreads Gore et al. 2009 Science Chia et al 2012 Nat Gen ✓⇡ n 1X i=1 1 i = S θπ ~ 8% pairwise diﬀ 1-S% pan-genome in ref

14. 4% of B73 absent ~8% absent 30% of the low copy sequence absent from reference genome %readsunmappedreads Gore et al. 2009 Science Chia et al 2012 Nat Gen ✓⇡ n 1X i=1 1 i = S θπ ~ 8% pairwise diﬀ 1-S% pan-genome in ref 0%# 20%# 40%# 60%# 80%# 100%# Angle# Length# NLB# SLB# Width# 10kb%RDV% Gene%RDV% HapMap2%genic% HapMap2%Intergenic% HapMap1%genic% HapMap1%Intergenic% 0# 2# 4# 6# 8# 10# 12# 14# 16# 18# 20# Angle# Length# NLB# SLB# Width# 0# 25# 30# 35# Intergenic# Intronic#SNPs# UTR# UP/Down#Stream# Syn#SNP# Splice#Site# NonSyn#SNP# 10Kb#RDV# A.# B.# C.# D.# 0%# 20%# 40%# 60%# 80%# 100%# Angle# Length# NLB# SLB# Width# 10kb%RDV% Gene%RDV% HapMap2%Intergenic% HapMap1%genic% 20# 25# 30# 35# lue#(Hlog10)# Intergenic# Intronic#SNPs# UTR# UP/Down#Stream# Syn#SNP# Splice#Site# NonSyn#SNP# 10Kb#RDV# Gene#RDV# A.# B. D.# 0%# 20%# 40%# 60%# 80%# 100%# Angle# Length# NLB# SLB# Width# 10kb%RDV% Gene%RDV% HapMap2%genic% HapMap2%Intergenic% HapMap1%genic% HapMap1%Interge 0# 2# 4# 6# 8# 10# 12# 14# 16# 18# 20# Angle# Length# NLB# 25# 30# 35# g10)# Intergenic# Intronic#SNPs# UTR# UP/Down#Stream# Syn#SNP# Splice#Site# NonSyn#SNP# 10Kb#RDV# Gene#RDV# A.# B.# D.# 0%# 20%# 40%# 60%# 80%# 100%# Angle# Length# NLB# SLB# Width# 10kb%RDV% Gene%RDV% HapMap2%genic% HapMap2%Intergenic% HapMap1%genic% HapMap1%Intergenic% 0# 2# 4# 6# 8# 10# 12# 14# 16# 18# 20# Angle# Length# NLB# SLB# Width# Intergenic 0# 0.5# 10# 15# 20# 25# 30# 35# pHvalue#(Hlog10)# Intergenic# Intronic#SNPs# UTR# UP/Down#Stream# Syn#SNP# Splice#Site# NonSyn#SNP# 10Kb#RDV# Gene#RDV# A.# B.# C.# D.# foldenrichment

15. hard sweep Hermisson & Pennings 2017 Meth Ecol Evol

18. hard sweep multiple mutations “soft” sweeps Hermisson & Pennings 2017 Meth Ecol Evol

19. hard sweep multiple mutations standing variation “soft” sweeps Hermisson & Pennings 2017 Meth Ecol Evol

20. hard sweep multiple mutations standing variation “soft” sweeps Θb=4ΝeμbL beneficial mutation rate genome size effective population size Hermisson & Pennings 2017 Meth Ecol Evol

21. hard sweep multiple mutations standing variation “soft” sweeps Θb=4ΝeμbL beneficial mutation rate genome size effective population size Hermisson & Pennings 2017 Meth Ecol Evol Θb<1 Θb>1

22. Beissinger et al. 2016 Nature Plants nucleotidediversity distance to nearest substitution (cM) prediction: bigger genomes have few hard sweeps

23. Beissinger et al. 2016 Nature Plants nucleotidediversity distance to nearest substitution (cM) prediction: bigger genomes have few hard sweeps

24. Sattah et al. 2011 PLoS Gen. Williamson et al. 2014 PLoS Gen Hernandez et al. 2011 Science Beissinger et al. 2016 Nature Plants L = 2,500 Mbp

25. Sattah et al. 2011 PLoS Gen. Williamson et al. 2014 PLoS Gen Hernandez et al. 2011 Science Beissinger et al. 2016 Nature Plants L = 2,500 Mbp diversity L = 220 Mbp

26. Sattah et al. 2011 PLoS Gen. Williamson et al. 2014 PLoS Gen Hernandez et al. 2011 Science Beissinger et al. 2016 Nature Plants L = 2,500 Mbp distance from substitution L = 3,100 Mbp L = 130 Mbp diversity L = 220 Mbp

27. M T G P H R L GGTCGAC ATG ACT GGT CCA CAT CGA CTG TAG

28. 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

29. 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

30. Hufford et al. 2012 Nat. Gen. Chia et al. 2012 Nat. Gen maizeteosinte prediction: bigger genomes have more intergenic (regulatory?) adaptation

31. Hufford et al. 2012 Nat. Gen. Chia et al. 2012 Nat. Gen maizeteosinte prediction: bigger genomes have more intergenic (regulatory?) adaptation

32. Hufford et al. 2012 Nat. Gen. Chia et al. 2012 Nat. Gen maizeteosinte prediction: bigger genomes have more intergenic (regulatory?) adaptation 5-10% selected regions do not include genes

33. Takuno et al. 2015 Genetics Low High common garden

34. Takuno et al. 2015 Genetics 39% 61% Intergenic Genic 19% 81% Standing Variation New mutation Low High common garden adaptive variants

35. Pyhäjärvi et al. GBE 2013 enrichment intergenic<——>coding Hancock et al 2011 Science environmental association allele freq. differentiation

36. Pyhäjärvi et al. GBE 2013 enrichment intergenic<——>coding Hancock et al 2011 Science enrichment no<———>yes intergenic synonymous nonsynonymous environmental association allele freq. differentiation

37. Mei et al. 2017 bioRxiv %adaptivenonsynonymous substitutions p=0.0075 prediction: big genomes have fewer adaptive nonsynonymous substitutions

38. ● ● ● ● 0 5 10 15 20 25 200 400 600 800 1000 Genome Size (Mb) OpenChromatinSize(Mb) Genome_feature ● Exon Intergenic Proximal Total_open_chromatin A ● ● 75% 80% 85% 90% 95% 500 1000 1500 2000 2500 Genome Size (Mb) %Non−exonicOpenChromatin Species ● ● ● ● ● ● ● ● ● Arabidopsis Brachypodium Cotton Maize Medicago Millet Rice Sorghum Tomato Tissue ● ● Callus Fiber Fruit Leaf Root Seedling Shoot B Genome Functional Space

39. ● ● ● ● 0 5 10 15 20 25 200 400 600 800 1000 Genome Size (Mb) OpenChromatinSize(Mb) Genome_feature ● Exon Intergenic Proximal Total_open_chromatin A ● ● 75% 80% 85% 90% 95% 500 1000 1500 2000 2500 Genome Size (Mb) %Non−exonicOpenChromatin Species ● ● ● ● ● ● ● ● ● Arabidopsis Brachypodium Cotton Maize Medicago Millet Rice Sorghum Tomato Tissue ● ● Callus Fiber Fruit Leaf Root Seedling Shoot B Genome Functional Space Functional Space Hard sweeps

40. ● ● ● ● 0 5 10 15 20 25 200 400 600 800 1000 Genome Size (Mb) OpenChromatinSize(Mb) Genome_feature ● Exon Intergenic Proximal Total_open_chromatin A ● ● 75% 80% 85% 90% 95% 500 1000 1500 2000 2500 Genome Size (Mb) %Non−exonicOpenChromatin Species ● ● ● ● ● ● ● ● ● Arabidopsis Brachypodium Cotton Maize Medicago Millet Rice Sorghum Tomato Tissue ● ● Callus Fiber Fruit Leaf Root Seedling Shoot B Genome Functional Space Functional Space Soft Sweeps Intergenic Adaptation Functional Space Hard sweeps

41. Acknowledgements UC Davis Graham Coop Wenbin Mei Dan Gates Markus Stetter Michelle Stitzer Plant Genome Research Program HiLo Lab Alumni Matt Hufford (Iowa State) Tanja Pyhäjärvi (Oulu) Shohei Takuno (Sokendai)

42. ● ● ● ● 0 5 10 15 20 25 200 400 600 800 1000 Genome Size (Mb) OpenChromatinSize(Mb) Genome_feature ● Exon Intergenic Proximal Total_open_chromatin A ● ● 75% 80% 85% 90% 95% 500 1000 1500 2000 2500 Genome Size (Mb) %Non−exonicOpenChromatin Species ● ● ● ● ● ● ● ● ● Arabidopsis Brachypodium Cotton Maize Medicago Millet Rice Sorghum Tomato Tissue ● ● Callus Fiber Fruit Leaf Root Seedling Shoot B Genome Functional Space

43. ● ● ● ● 0 5 10 15 20 25 200 400 600 800 1000 Genome Size (Mb) OpenChromatinSize(Mb) Genome_feature ● Exon Intergenic Proximal Total_open_chromatin A ● ● 75% 80% 85% 90% 95% 500 1000 1500 2000 2500 Genome Size (Mb) %Non−exonicOpenChromatin Species ● ● ● ● ● ● ● ● ● Arabidopsis Brachypodium Cotton Maize Medicago Millet Rice Sorghum Tomato Tissue ● ● Callus Fiber Fruit Leaf Root Seedling Shoot B Genome Functional Space Functional Space Hard sweeps

44. ● ● ● ● 0 5 10 15 20 25 200 400 600 800 1000 Genome Size (Mb) OpenChromatinSize(Mb) Genome_feature ● Exon Intergenic Proximal Total_open_chromatin A ● ● 75% 80% 85% 90% 95% 500 1000 1500 2000 2500 Genome Size (Mb) %Non−exonicOpenChromatin Species ● ● ● ● ● ● ● ● ● Arabidopsis Brachypodium Cotton Maize Medicago Millet Rice Sorghum Tomato Tissue ● ● Callus Fiber Fruit Leaf Root Seedling Shoot B Genome Functional Space Functional Space Soft Sweeps Intergenic Adaptation Functional Space Hard sweeps

Adaptation in plant genomes: bigger is different

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