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Adaptation in plant genomes: bigger is different

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Here we have proposed the functional space hypothesis, positing that mutational target size scales with genome size, impacting the number, source, and genomic location of beneficial mutations that contribute to adaptation. Though motivated by preliminary evidence, mostly from Arabidopsis and maize, more data are needed before any rigorous assessment of the hypothesis can be made. If correct, the functional space hypothesis suggests that we should expect plants with large genomes to exhibit more functional mutations outside of genes, more regulatory variation, and likely less signal of strong selective sweeps reducing diversity. These differences have implications for how we study the evolution and development of plant genomes, from where we should look for signals of adaptation to what patterns we expect adaptation to leave in genetic diversity or gene expression data. While flowering plant genomes vary across more than three orders of magnitude in size, most studies of both functional and evolutionary genomics have focused on species at the extreme small edge of this scale. Our hypothesis predicts that methods and results from these small genomes may not replicate well as we begin to explore large plant genomes. Finally, while we have focused here on evidence from plant genomes, we see no a priori reason why similar arguments might not hold in other taxa as well.

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Adaptation in plant genomes: bigger is different

  1. 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. 2. Brandon Gaut log haploid genome size Zea maysA. thaliana #species
  3. 3. Brandon Gaut log haploid genome size Zea maysA. thaliana #species Springer et al. (2016) Plant Cell 1 Megabase DNA maize Arabidopsis
  4. 4. Lloyd et al. 2017 bioRxiv A .thaliana functional prediction
  5. 5. Lloyd et al. 2017 bioRxiv A .thaliana functional prediction
  6. 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. 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. 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. 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. 10. Doebley 2004, Studer et al. 2011 tb1 Hopscotch ZmCCT CACTA Yang et al. 2013 plant architecture flowering time
  11. 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. 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. 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. 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. 15. hard sweep Hermisson & Pennings 2017 Meth Ecol Evol
  16. 16. hard sweep Hermisson & Pennings 2017 Meth Ecol Evol
  17. 17. hard sweep Hermisson & Pennings 2017 Meth Ecol Evol
  18. 18. hard sweep multiple mutations “soft” sweeps Hermisson & Pennings 2017 Meth Ecol Evol
  19. 19. hard sweep multiple mutations standing variation “soft” sweeps Hermisson & Pennings 2017 Meth Ecol Evol
  20. 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. 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. 22. Beissinger et al. 2016 Nature Plants nucleotidediversity distance to nearest substitution (cM) prediction: bigger genomes have few hard sweeps
  23. 23. Beissinger et al. 2016 Nature Plants nucleotidediversity distance to nearest substitution (cM) prediction: bigger genomes have few hard sweeps
  24. 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. 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. 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. 27. M T G P H R L GGTCGAC ATG ACT GGT CCA CAT CGA CTG TAG
  28. 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. 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. 30. Hufford et al. 2012 Nat. Gen. Chia et al. 2012 Nat. Gen maizeteosinte prediction: bigger genomes have more intergenic (regulatory?) adaptation
  31. 31. Hufford et al. 2012 Nat. Gen. Chia et al. 2012 Nat. Gen maizeteosinte prediction: bigger genomes have more intergenic (regulatory?) adaptation
  32. 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. 33. Takuno et al. 2015 Genetics Low High common garden
  34. 34. Takuno et al. 2015 Genetics 39% 61% Intergenic Genic 19% 81% Standing Variation New mutation Low High common garden adaptive variants
  35. 35. Pyhäjärvi et al. GBE 2013 enrichment intergenic<——>coding Hancock et al 2011 Science environmental association allele freq. differentiation
  36. 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. 37. Mei et al. 2017 bioRxiv %adaptivenonsynonymous substitutions p=0.0075 prediction: big genomes have fewer adaptive nonsynonymous substitutions
  38. 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. 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. 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. 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. 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. 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. 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

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