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Adaptive evolution of genome size across altitudinal clines in maize

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Genome size in plants can vary by orders of magnitude, but this variation has long been considered to be of little to no functional consequence.
Studying three independent adaptations to high elevation in Zea mays, we find that genome size experiences parallel pressure from natural selection, causing a linear reduction in genome size with increasing altitude.
Though reductions in repetitive content are responsible for the genome size change, we find that repeats are not targeted uniformly, but that the same repetitive sequences are removed as Z. mays taxa move to higher altitude.
To identify the phenotype influenced by genome size, we study how 20% variation in genome size in a single teosinte population impacts leaf growth.
We find that genome size variation correlates negatively with cell production rate but not cell size, suggesting that individuals with larger genomes require longer to complete a mitotic cycle.
We reanalyze data from maize inbreds to show that slower cell production can lead to a delay in flowering time, suggesting that genome size can be used as a developmental clock to help adapt maize to different altitudes.

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Adaptive evolution of genome size across altitudinal clines in maize

  1. 1. Jeffrey Ross-Ibarra @jrossibarra • www.rilab.org Plant Sciences • Center for Population Biology • Genome Center University of California Davis Adaptive Clines in Genome Size in Maize
  2. 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
  3. 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
  4. 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
  5. 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
  6. 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
  7. 7. Lynch and Connnery (2003) Science
  8. 8. Lynch and Connnery (2003) Science Lefébure et al. (2017) Genome Research genome size (pg)dN/dS surface subterannean
  9. 9. Whitney et al. (2010) Evolution Contrast in Ne ContrastinGenomeSize
  10. 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. 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. 12. 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
  13. 13. Paul Bilinski Jeremy Berg Mark Grote Patrice Albert Anne Lorant
  14. 14. Brandon Gaut log haploid genome size Zea maysA. thaliana #species
  15. 15. Brandon Gaut log haploid genome size Zea maysA. thaliana #species Springer et al. (2016) Plant Cell 1 Megabase DNA maize Arabidopsis
  16. 16. Brandon Gaut log haploid genome size Zea maysA. thaliana #species landrace diploidgenomesize Díez et al. (2013) New Phyt Springer et al. (2016) Plant Cell 1 Megabase DNA maize Arabidopsis
  17. 17. Z. mays ssp. parviglumis Z. mays ssp. mexicana Pyhäjärvi et al. (2013) GBE
  18. 18. 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
  19. 19. 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
  20. 20. 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
  21. 21. 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
  22. 22. altitude GenomeSize(Mb) 77 landraces S. America Mexico parviglumis mexicana teosinte altitude3250 3125 3000 2875 2750
  23. 23. altitude GenomeSize(Mb) 77 landraces S. America Mexico teosinte 95 mexicana altitude
  24. 24. altitude GenomeSize(Mb) 77 landraces S. America Mexico teosinte 95 mexicana altitude genome size (bp) #individuals h2~0.9
  25. 25. 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
  26. 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 landraces landraces Kinship Additive Genetic Var.
  27. 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. -110Kb/m -260Kb/m
  28. 28. Rosado et al. (2005) Maize Genetics Newsletter (shh, secret) Knob180 KnobTR1 Maize TEs Sorghum TEs Jiao et al. (2017) Nature copy number
  29. 29. Rosado et al. (2005) Maize Genetics Newsletter (shh, secret) Knob180 KnobTR1 Maize TEs Sorghum TEs Jiao et al. (2017) Nature copy number
  30. 30. Rosado et al. (2005) Maize Genetics Newsletter (shh, secret) Knob180 KnobTR1 Maize TEs Sorghum TEs Jiao et al. (2017) Nature copy number
  31. 31. r2=0.77 r2=0.74
  32. 32. P = µ + alt ⇤ A + GS ⇤ GS + g + " g ⇠ MV N (0, VAK) " ⇠ N (0, V✏) AltitudeRepeat Genome Size as Covariate Additive Component
  33. 33. altitude B-repeatreads Masonbrink et al. (2013) Genetics B chromosome
  34. 34. altitude MbTE maize mexicana S. America Mexico Region
  35. 35. altitude MbTE Tenaillon et al.(2011) GBE maizeZ.luxurians relative abundance of TE families maize mexicana S. America Mexico Region
  36. 36. results: total, among TEs, B Knobabundance(Mb) altitude knob180 maize mexicana maize mexicana S. Am. Mexico Region knobTR1
  37. 37. results: total, among TEs, B Knobabundance(Mb) altitude knob180 Photo by Kelly Dawe maize mexicana maize mexicana S. Am. Mexico Region knobTR1
  38. 38. 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
  39. 39. 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.
  40. 40. Bennett (1972) Proc Roy Soc B #species cellcycletime(h) annual perennial annual perennial genome size (pg of 3C)
  41. 41. 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
  42. 42. mother(n=202plants) genome size
  43. 43. Šímová and Herben (2012) Proc Roy Soc B Walker and Smith (2002) Development
  44. 44. 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
  45. 45. 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
  46. 46. 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
  47. 47. 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
  48. 48. Leiboff et al. (2015) Nat Comm cell number (cell division rate)floweringtime growth stage
  49. 49. Tenaillon et al. (2016) PeerJ leafelongationrate genome size early-flowering flints late-flowering tropical
  50. 50. 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
  51. 51. large small GENOME SIZE
  52. 52. large small GENOME SIZE slow fast CELL DIVISION Density of βGS
  53. 53. large small GENOME SIZE late early FLOWERING TIME slow fast CELL DIVISION Density of βGS
  54. 54. 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
  55. 55. Acknowledgements UC Davis U Georgia U Missouri Patrice Albert Jim Birchler Jeremy Berg Paul Bilinski Graham Coop Mark Grote Anne Lorant Juvenal Quesada Jinliang Yang Kelly Dawe Ed Buckler Sherry Flint-Garcia USDA Cornell Kelly Swarts Plant Genome Research Program HiLo
  56. 56. large small GENOME SIZE late early FLOWERING TIME slow fast CELL DIVISION Density of βGS

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