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Parallel altitudinal clines reveal trends adaptive evolution of genome size in Zea mays

Paul Bilinski, Patrice S. Albert, Jeremy J Berg, James A Birchler, Mark Grote, Anne Lorant, Juvenal Quezada, Kelly Swarts, Jinliang Yang, Jeffrey Ross-Ibarra
doi: https://doi.org/10.1101/134528
Paul Bilinski
1Dept. of Plant Sciences, University of California, Davis, CA, USA
2Research Group for Ancient Genomics and Evolution, Dept. of Molecular Biology, Max Planck Institute for Developmental Biology, Tuebingen, DE
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Patrice S. Albert
3Dept. of Biological Sciences, University of Missouri, Columbia, MO, USA
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Jeremy J Berg
4Center for Population Biology, University of California, Davis, CA, USA
5Dept. of Evolution and Ecology, University of California, Davis, CA, USA
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James A Birchler
3Dept. of Biological Sciences, University of Missouri, Columbia, MO, USA
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Mark Grote
6Dept. of Anthropology, University of California, Davis, CA, USA
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Anne Lorant
1Dept. of Plant Sciences, University of California, Davis, CA, USA
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Juvenal Quezada
1Dept. of Plant Sciences, University of California, Davis, CA, USA
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Kelly Swarts
2Research Group for Ancient Genomics and Evolution, Dept. of Molecular Biology, Max Planck Institute for Developmental Biology, Tuebingen, DE
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Jinliang Yang
1Dept. of Plant Sciences, University of California, Davis, CA, USA
7Dept. of Horticulture and Agronomy, University of Nebraska, Lincoln, NE, USA
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Jeffrey Ross-Ibarra
1Dept. of Plant Sciences, University of California, Davis, CA, USA
3Dept. of Biological Sciences, University of Missouri, Columbia, MO, USA
8Genome Center, University of California, Davis, CA, USA
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Abstract

While the vast majority of genome size variation in plants is due to differences in repetitive sequence, we know little about how selection acts on repeat content in natural populations. Here we investigate parallel changes in intraspecific genome size and repeat content of domesticated maize (Zea mays) landraces and their wild relative teosinte across altitudinal gradients in Mesoamerica and South America. We combine genotyping, low coverage whole-genome sequence data, and flow cytometry to test for evidence of selection on genome size and individual repeat abundance. We find that population structure alone cannot explain the observed variation, implying that clinal patterns of genome size are maintained by natural selection. Our modeling additionally provides evidence of selection on individual heterochromatic knob repeats, likely due to their large individual contribution to genome size. To better understand the phenotypes driving selection on genome size, we conducted a growth chamber experiment using a population of highland teosinte exhibiting extensive variation in genome size. We find weak support for a positive correlation between genome size and cell size, but stronger support for a negative correlation between genome size and the rate of cell production. Reanalyzing published data of cell counts in maize shoot apical meristems, we then identify a negative correlation between cell production rate and flowering time. Together, our data suggest a model in which variation in genome size is driven by natural selection on flowering time across altitudinal clines, connecting intraspecific variation in repetitive sequence to important differences in adaptive phenotypes.

Author summary 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 altitude in Zea mays, we find that genome size experiences parallel pressures 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 only those individual loci contributing most to the variation in genome size are individually targeted by selection. To identify the phenotype influenced by genome size, we study how variation in genome size within a single teosinte population impacts leaf growth and cell division. We find that genome size variation correlates negatively with the rate of cell division, suggesting that individuals with larger genomes require longer to complete a mitotic cycle. Finally, we reanalyze data from maize inbreds to show that faster cell division is correlated with earlier flowering, connecting observed variation in genome size to an important adaptive phenotype.

Footnotes

  • ↵* E-mail: rossibarra{at}ucdavis.edu, rossibarra{at}ucdavis.edu

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted July 13, 2017.
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Parallel altitudinal clines reveal trends adaptive evolution of genome size in Zea mays
Paul Bilinski, Patrice S. Albert, Jeremy J Berg, James A Birchler, Mark Grote, Anne Lorant, Juvenal Quezada, Kelly Swarts, Jinliang Yang, Jeffrey Ross-Ibarra
bioRxiv 134528; doi: https://doi.org/10.1101/134528
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Parallel altitudinal clines reveal trends adaptive evolution of genome size in Zea mays
Paul Bilinski, Patrice S. Albert, Jeremy J Berg, James A Birchler, Mark Grote, Anne Lorant, Juvenal Quezada, Kelly Swarts, Jinliang Yang, Jeffrey Ross-Ibarra
bioRxiv 134528; doi: https://doi.org/10.1101/134528

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