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Adaptive evolution of genome size across altitudinal clines in maize

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.

Adaptive evolution of genome size across altitudinal clines in maize

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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
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
By Nr387241 - Own work, CC BY-SA 3.0, https://
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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
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copyleft/fdl.html)], via Wikimedia Commons
Protopterus (130Gb)
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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
Genlisea (0.065Gb)
By Michal Rubeš [CC BY 3.0 cz
(http://creativecommons.org/
licenses/by/3.0/cz/deed.en)], via
Wikimedia Commons
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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
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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
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Adaptive evolution of genome size across altitudinal clines in maize

  • 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. 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. 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. 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. 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. 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. 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. 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. Paul Bilinski Jeremy Berg Mark Grote Patrice Albert Anne Lorant
  • 14. Brandon Gaut log haploid genome size Zea maysA. thaliana #species
  • 15. Brandon Gaut log haploid genome size Zea maysA. thaliana #species Springer et al. (2016) Plant Cell 1 Megabase DNA maize Arabidopsis
  • 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
  • 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
  • 30. Rosado et al. (2005) Maize Genetics Newsletter (shh, secret) Knob180 KnobTR1 Maize TEs Sorghum TEs Jiao et al. (2017) Nature copy number
  • 31. Rosado et al. (2005) Maize Genetics Newsletter (shh, secret) Knob180 KnobTR1 Maize TEs Sorghum TEs Jiao et al. (2017) Nature copy number
  • 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
  • 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
  • 44. 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
  • 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. 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