Genome size and adaptation in plants

1. Jeffrey Ross-Ibarra @jrossibarra • www.rilab.org Plant Sciences • Center for Population Biology • Genome Center University of California Davis Embiggening DNA: the role of plant genome size in intra- and interspeciﬁc adaptation

2. Abizar at English Wikipedia [CC BY-SA 3.0 (http://creativecommons.org/licenses/by-sa/3.0) or GFDL (http://www.gnu.org/copyleft/fdl.html)], via Wikimedia Commons Genome Size (bp)

3. By Nr387241 - Own work, CC BY-SA 3.0, https:// commons.wikimedia.org/w/index.php? curid=14945255 Mycoplasma (0.0006Gb) Abizar at English Wikipedia [CC BY-SA 3.0 (http://creativecommons.org/licenses/by-sa/3.0) or GFDL (http://www.gnu.org/copyleft/fdl.html)], via Wikimedia Commons Genome Size (bp)

4. By Gőtehal.jpg: Mathae derivative work: Bff (Gőtehal.jpg) [CC BY 2.5 (http:// creativecommons.org/licenses/by/2.5), CC-BY-SA-3.0 (http:// creativecommons.org/licenses/by-sa/3.0/) or GFDL (http://www.gnu.org/ copyleft/fdl.html)], via Wikimedia Commons Protopterus (130Gb) By Nr387241 - Own work, CC BY-SA 3.0, https:// commons.wikimedia.org/w/index.php? curid=14945255 Mycoplasma (0.0006Gb) Abizar at English Wikipedia [CC BY-SA 3.0 (http://creativecommons.org/licenses/by-sa/3.0) or GFDL (http://www.gnu.org/copyleft/fdl.html)], via Wikimedia Commons Genome Size (bp)

5. Genlisea (0.065Gb) By Michal Rubeš [CC BY 3.0 cz (http://creativecommons.org/ licenses/by/3.0/cz/deed.en)], via Wikimedia Commons By Gőtehal.jpg: Mathae derivative work: Bff (Gőtehal.jpg) [CC BY 2.5 (http:// creativecommons.org/licenses/by/2.5), CC-BY-SA-3.0 (http:// creativecommons.org/licenses/by-sa/3.0/) or GFDL (http://www.gnu.org/ copyleft/fdl.html)], via Wikimedia Commons Protopterus (130Gb) By Nr387241 - Own work, CC BY-SA 3.0, https:// commons.wikimedia.org/w/index.php? curid=14945255 Mycoplasma (0.0006Gb) Abizar at English Wikipedia [CC BY-SA 3.0 (http://creativecommons.org/licenses/by-sa/3.0) or GFDL (http://www.gnu.org/copyleft/fdl.html)], via Wikimedia Commons Genome Size (bp)

6. By alpsdake - Own work, CC0, https://commons.wikimedia.org/w/index.php? curid=12228596 Paris (150Gb) Genlisea (0.065Gb) By Michal Rubeš [CC BY 3.0 cz (http://creativecommons.org/ licenses/by/3.0/cz/deed.en)], via Wikimedia Commons By Gőtehal.jpg: Mathae derivative work: Bff (Gőtehal.jpg) [CC BY 2.5 (http:// creativecommons.org/licenses/by/2.5), CC-BY-SA-3.0 (http:// creativecommons.org/licenses/by-sa/3.0/) or GFDL (http://www.gnu.org/ copyleft/fdl.html)], via Wikimedia Commons Protopterus (130Gb) By Nr387241 - Own work, CC BY-SA 3.0, https:// commons.wikimedia.org/w/index.php? curid=14945255 Mycoplasma (0.0006Gb) Abizar at English Wikipedia [CC BY-SA 3.0 (http://creativecommons.org/licenses/by-sa/3.0) or GFDL (http://www.gnu.org/copyleft/fdl.html)], via Wikimedia Commons Genome Size (bp)

7. Lynch and Connnery (2003) Science

8. Lynch and Connnery (2003) Science Lefébure et al. (2017) Genome Research genome size (pg)dN/dS surface subterannean

9. Whitney et al. (2010) Evolution Contrast in Ne ContrastinGenomeSize

10. Seed Weight (+) Leaf Size (-) Knight (2005) Ann Bot Genome Size (2C pg) Seed Weight GenomeSize(2Cpg)specificleafarea Whitney et al. (2010) Evolution Contrast in Ne ContrastinGenomeSize

11. Kang et al. (2015) Sci Reports GenomeSize SoilNitrogen Seed Weight (+) Leaf Size (-) Knight (2005) Ann Bot Primulinaspp. Genome Size (2C pg) Seed Weight GenomeSize(2Cpg)specificleafarea Whitney et al. (2010) Evolution Contrast in Ne ContrastinGenomeSize

12. Larger genomes adapt differently: the “functional space” hypothesis Intraspeciﬁc adaptive evolution of genome size in maize

13. Larger genomes adapt differently: the “functional space” hypothesis Intraspeciﬁc adaptive evolution of genome size in maize

14. The small differences in genome size within species seem generally to be of minor importance compared to other components of plant fitness. Šmarda & Petr Bureš (2010) Preslia The ‘plastic genome’ seems to be an idea rather than a defendable scientific hypothesis; intraspecific variation is less frequent than presently thought. Greilhuber (1998) Ann Bot

15. maizeteosinte

16. landrace diploidgenomesize Díez et al. (2013) New Phyt

18. Z. mays ssp. parviglumis Z. mays ssp. mexicana Pyhäjärvi et al. (2013) GBE

19. Domestication 10,000BP Takuno et al. (2015) Genetics Lowland K=3K=4 Highland Lowland Highland Mesoamerica South America Lowland A B K=2K=3K=4 Highland Lowland Highland Mesoamerica South America Altitude

20. Domestication 10,000BP Mexican Highlands 6,000BP Takuno et al. (2015) Genetics Lowland K=3K=4 Highland Lowland Highland Mesoamerica South America Lowland A B K=2K=3K=4 Highland Lowland Highland Mesoamerica South America Altitude

21. Domestication 10,000BP Mexican Highlands 6,000BP S. American lowlands 6,000BP Takuno et al. (2015) Genetics Lowland K=3K=4 Highland Lowland Highland Mesoamerica South America Lowland A B K=2K=3K=4 Highland Lowland Highland Mesoamerica South America Altitude

22. Domestication 10,000BP Mexican Highlands 6,000BP S. American lowlands 6,000BP Andes 4,000BP Takuno et al. (2015) Genetics Lowland K=3K=4 Highland Lowland Highland Mesoamerica South America Lowland A B K=2K=3K=4 Highland Lowland Highland Mesoamerica South America Altitude

23. altitude GenomeSize(Mb) 77 landraces S. America Mexico parviglumis mexicana teosinte altitude3250 3125 3000 2875 2750

24. altitude GenomeSize(Mb) 77 landraces S. America Mexico teosinte 95 mexicana altitude

25. altitude GenomeSize(Mb) 77 landraces S. America Mexico teosinte 95 mexicana altitude genome size (bp) #individuals h2~0.9

26. altitude GenomeSize(Mb) 77 landraces S. America Mexico teosinte 95 mexicana altitude P = µ + alt ⇤ A + g + " g ⇠ MV N (0, VAK) " ⇠ N (0, V✏) Genome Size Altitude Additive Component Berg and Coop (2014) Plos Gen

27. altitude GenomeSize(Mb) 77 landraces S. America Mexico teosinte 95 mexicana altitude P = µ + alt ⇤ A + g + " g ⇠ MV N (0, VAK) " ⇠ N (0, V✏) Genome Size Altitude Additive Component Berg and Coop (2014) Plos Gen landraces landraces Kinship Additive Genetic Var.

28. altitude GenomeSize(Mb) 77 landraces S. America Mexico teosinte 95 mexicana altitude P = µ + alt ⇤ A + g + " g ⇠ MV N (0, VAK) " ⇠ N (0, V✏) Genome Size Altitude Additive Component Berg and Coop (2014) Plos Gen landraces landraces Kinship Additive Genetic Var. -110Kb/m -260Kb/m

29. Rosado et al. (2005) Maize Genetics Newsletter (shh, secret) Knob180 KnobTR1 Maize TEs Sorghum TEs Jiao et al. (2017) Nature copy number

32. r2=0.77 r2=0.74

33. P = µ + alt ⇤ A + GS ⇤ GS + g + " g ⇠ MV N (0, VAK) " ⇠ N (0, V✏) AltitudeRepeat Genome Size as Covariate Additive Component

34. altitude B-repeatreads Masonbrink et al. (2013) Genetics B chromosome

35. altitude MbTE maize mexicana S. America Mexico Region

36. altitude MbTE Tenaillon et al.(2011) GBE maizeZ.luxurians relative abundance of TE families maize mexicana S. America Mexico Region

37. results: total, among TEs, B Knobabundance(Mb) altitude knob180 maize mexicana maize mexicana S. Am. Mexico Region knobTR1

38. results: total, among TEs, B Knobabundance(Mb) altitude knob180 Photo by Kelly Dawe maize mexicana maize mexicana S. Am. Mexico Region knobTR1

39. results: total, among TEs, B Knobabundance(Mb) altitude knob180 Kanizay et al. (2013) Heredity altitude maize mexicana parviglumis subspecies Ab10frequency maize mexicana maize mexicana S. Am. Mexico Region knobTR1

40. Nature Education 2013 https://www.nature.com/scitable/content/ne0000/ne0000/ne0000/ne0000/113371527/14707478.jpg DNA Replication Francis et al. (2008) Ann Bot FIG. 2. DNA C-value (pg) and cell cycle time (h) in the root apic istem of a range of (A) eudicots and monocots (n ¼ 110), and (B) e (n ¼ 60). See Table 2 for regression analyses.

41. Bennett (1972) Proc Roy Soc B #species cellcycletime(h) annual perennial annual perennial genome size (pg of 3C)

42. 0 10 20 30 40 60 80 100 120 days to pollen count subpsecies parviglumis mexicana Rodriguez et al. (2006) Maydica Highﬂowering time (days) #plants SAm Mex SAm Mex Low Flint-Garcia et al. (unpublished) ﬂoweringtime(days) mexicana parviglumis

43. mother(n=202plants) genome size

44. Šímová and Herben (2012) Proc Roy Soc B Walker and Smith (2002) Development

45. Leaf Elongation (LER) Cell Size (CS) Cell Production (CP) Genome Size (GS) + - Šímová and Herben (2012) Proc Roy Soc B Walker and Smith (2002) Development

46. Leaf Elongation (LER) Cell Size (CS) Cell Production (CP) Genome Size (GS) + - log(CS) = 0 + GS ⇤ log(GS) Posterior Density of γGS Šímová and Herben (2012) Proc Roy Soc B Walker and Smith (2002) Development

47. Leaf Elongation (LER) Cell Size (CS) Cell Production (CP) Genome Size (GS) + - log(LER) = ⌧0 + ⌧GS ⇤ log(GS) log(CS) = 0 + GS ⇤ log(GS) GS = ⌧GS GS Posterior Density of γGS Šímová and Herben (2012) Proc Roy Soc B Walker and Smith (2002) Development

48. Leaf Elongation (LER) Cell Size (CS) Cell Production (CP) Genome Size (GS) + - log(CP) = 0 + GS ⇤ log(GS) log(LER) = ⌧0 + ⌧GS ⇤ log(GS) log(CS) = 0 + GS ⇤ log(GS) GS = ⌧GS GS Posterior Density of βGS Posterior Density of γGS Šímová and Herben (2012) Proc Roy Soc B Walker and Smith (2002) Development

49. Leiboff et al. (2015) Nat Comm cell number (cell division rate)ﬂoweringtime growth stage

50. Tenaillon et al. (2016) PeerJ leafelongationrate genome size early-flowering flints late-flowering tropical

51. 0 10 20 30 100 105 110 DNA plants cyc relative genome size late ﬂowering gen 0 early ﬂowering gen 6 #Plants Rayburn et al. (1994) Plant Breeding Tenaillon et al. (2016) PeerJ leafelongationrate genome size early-flowering flints late-flowering tropical

52. large small GENOME SIZE

53. large small GENOME SIZE slow fast CELL DIVISION Density of βGS

54. large small GENOME SIZE late early FLOWERING TIME slow fast CELL DIVISION Density of βGS

55. 1. Selection for earlier flowering leads to smaller genomes across altitudinal gradients in maize and teosinte 2. Genome size is a quantitative trait that can affect fitness, and observed intraspecific variation may be adaptive 3. Selection on genome size likely impacts the evolution of individual repeat classes

56. Intraspeciﬁc adaptive evolution of genome size in maize Larger genomes adapt differently: the “functional space” hypothesis https://github.com/RILAB/AJB_MutationalTargetSize_GenomeSize

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

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

59. Lloyd et al. 2017 bioRxiv functional prediction

60. Lloyd et al. 2017 bioRxiv functional prediction

61. Lloyd et al. 2017 bioRxiv 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.)

62. ● ● ● ● 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.)

63. 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

64. 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

65. hard sweep Hermisson & Pennings 2017 Meth Ecol Evol

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

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

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

71. 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

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

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

74. 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

75. 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

76. 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

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

78. 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

79. 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

80. Hufford et al. 2012 Nat. Gen. Chia et al. 2012 Nat. Gen maizeteosinte prediction: bigger genomes have more intergenic adaptation

81. Hufford et al. 2012 Nat. Gen. Chia et al. 2012 Nat. Gen maizeteosinte prediction: bigger genomes have more intergenic adaptation

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

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

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

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

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

87. Mei et al. 2017 bioRxiv %adaptivenonsynonymous substitutions p=0.0075

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

89. Fedoroff 2012, Wang and Dooner 2006

90. Fedoroff 2012, Wang and Dooner 2006 Homologous (loop) 34% No pairing 20%Nonhomologous 46% Maguire 1966 Genetics

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

92. 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

93. 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

94. 4% of B73 absent ~8% absent %readsunmappedreads Gore et al. 2009 Science Chia et al 2012 Nat Gen

95. 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

96. 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

97. ● ● ● ● 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

98. ● ● ● ● 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

99. ● ● ● ● 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

100. • Genome size is the best quantitative trait in the galaxy, and may itself be an adaptive trait • Selection on genome size may impact repeat evolution • Large genomes may have a larger mutational target — more “functional space” — and thus adapt via soft sweeps and noncoding variation • Consider genome size when designing and interpreting studies of plant adaptation Concluding Thoughts on Embiggening Plant DNA Kew C-Value Database

101. Acknowledgements USDA Ed Buckler Doreen Ware U Missouri Patrice Albert Jim Birchler U Georgia Kelly Dawe Cornell Kelly Swarts UC Davis Jeremy Berg Graham Coop Mark Grote Juvenal Quesada Plant Genome Research Program HiLo Lab Alumni Tim Beissinger (USDA-ARS, Mizzou) Paul Bilinski Kate Crosby (Monsanto) Matt Hufford (Iowa State) Tanja Pyhäjärvi (Oulu) Shohei Takuno (Sokendai) Joost van Heerwaarden (Wageningen) Jinliang Yang (U Nebraska-Lincoln)

103. ● ● ● ● 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 Genom Functional Space Functional Space Soft Sweeps Intergenic Adaptation Functional Space Hard sweeps

104. END

105. standing variation ©2011NatureAmeric NATURE GENETICS ADVANCE ONLINE PUBLICATION 3 mutation rate21, strongly suggesting that the Hopscotch insertion (and thus, the older Tourist as well) existed as standing genetic variation in the teosinte ancestor of maize. Thus, we conclude that the Hopscotch insertion likely predated domestication by more than 10,000 years and the Tourist insertion by an even greater amount of time. We identified four fixed differences in the portion of the proximal and distal components of the control region that show evidence of selection. We used transient assays in maize leaf protoplasts to test all four differences for effects on gene expression. Maize and teosinte chromosomal segments for the portions of the proximal and distal components with these four differences were cloned into reporter constructs upstream of the minimal promoter of the cauliflower mosaic virus (mpCaMV), the firefly luciferase ORF and the nopaline synthase (NOS) terminator (Fig. 4). Each construct was assayed for luminescence after transformation by electroporation into maize protoplast. The constructs for the distal component contrast the effects of the Tourist insertion plus the single fixed nucleotide substitution that distinguish maize and teosinte. Both the maize and teosinte constructs 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 nucleotide 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 construct 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 Figure 4 Constructs and corresponding normalized luciferase expression levels. Transient assays were performed in maize leaf protoplast. Each construct is drawn to scale. The construct backbone consists of the minimal promoter from the cauliflower mosaic virus (mpCaMV, gray box), luciferase ORF (luc, white box) and the nopaline synthase terminator (black box). Portions of the proximal and distal components of the control region (hatched boxes) from maize and teosinte were cloned into restriction sites upstream of the minimal promoter. “ ” denotes the excision of either the Tourist or Hopscotch element from the maize construct. Horizontal green bars show the normalized mean with s.e.m. for each construct. relative expressionconstruct Studer et al. 2011 Nat. Gen.; Vann et al. 2015 enhances expression teosinte branched - tb1

106. hard sweep Figure 1. Phenotypes. a. Maize ear showing the cob (cb) exposed at top. b. Teosinte ear with the rachis internode (in) and glume (gl) labeled. c. Teosinte ear from a plant with a maize allele of tga1 Wang et al. Page 10 NIH-PAAuthorManuscriptNIH-PAAuthorManuscript Wang et al. 2015 Genetics protein change teosinte glume architecture - tga1

107. Makarevitch et al. 2015 PLoS Genetics

108. Makarevitch et al. 2015 PLoS Genetics single TE family many genes

109. Makarevitch et al. 2015 PLoS Genetics single TE family many genes new 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) on Septemhttp://biorxiv.org/Downloaded from 0.5 1.0 1.5 2.0 2.5 3.0 3.5 Oh43 B73 Mo17 (stress/control) 0% 20% 40% 60% 80% 100% alaw dagaf etug flip gyma ipiki jeli joemon naiba nihep odoj pebi raider riiryl ubel uwum Zm00346 Zm02117 Zm03238 Zm05382 Salt UV Heat Cold B A Percentofconserved genes on September 9, 2014http://biorxiv.org/Downloaded from * ** *** * * single gene, many individuals

110. Doebley 2004, Studer et al., 2011 tb1 Hopscotch

111. Doebley 2004, Studer et al., 2011 tb1 Hopscotch ZmCCT CACTA Yang et al., 2013

112. Mu KNOTTED1 kn1 Greene, et al., 1994 http://pmb.berkeley.edu/sites/default/ﬁles/users/Knotted1%20mutant.jpgDoebley 2004, Studer et al., 2011 tb1 Hopscotch ZmCCT CACTA Yang et al., 2013

Genome size and adaptation in plants

Genome size and adaptation in plants

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