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

PLoS Genet. 2018 May 10;14(5):e1007162. doi: 10.1371/journal.pgen.1007162. eCollection 2018 May.

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.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Adaptation, Physiological / genetics
  • Altitude
  • Central America
  • Evolution, Molecular*
  • Genetic Variation
  • Genome Size*
  • Genome, Plant / genetics*
  • Geography
  • In Situ Hybridization, Fluorescence
  • Repetitive Sequences, Nucleic Acid / genetics
  • Selection, Genetic
  • South America
  • Species Specificity
  • Zea mays / classification
  • Zea mays / genetics*

Grants and funding

We acknowledge financial support from United States National Science Foundation grants IOS-0922703 and IOS-1238014 and the US Department of Agriculture Hatch project CA-D-PLS-2066-H (JRI). P.B. would like to thank the UC MEXUS (http://ucmexus.ucr.edu/) Dissertation Grant, DuPont Pioneer, and the UC Davis Department of Plant Sciences for funding and support. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.