Departures from Mendelian inheritance of EPSPS gene copies in a herbicide-resistant weed

Abstract

Mendelian transmission requires a stable genetic structure, but unstable elements contribute to dynamic genomes. Here, we report on non-Mendelian inheritance and intra-individual instability of extrachromosomal gene copies, which are associated with rapid evolution of herbicide resistance in the dioecious, agricultural weed Amaranthus palmeri. Copy number variation for the glyphosate resistance gene EPSPS was quantified using digital droplet PCR within individuals, and for parents and offspring of controlled crosses with copy number ranging from 1 to [~]160. Parent-offspring regressions of copy number indicates non-Mendelian inheritance. Heritability is higher (hG2=1.60) below [~]33 copies, than above (hG2=0.22) because parents with fewer gene copies yield offspring with similar or increased mean copy number, whereas offspring of high copy number parents have fewer copies than parents. Intra-individual variance in copy number increased with mean individual copy number, likely contributing to variation observed in offspring copy number, but not sufficient to explain the most extreme transgressive copy number variants, nor the loss of high copy number. In short, copy number is less stable and less heritable in parents with more EPSPS copies, with offspring losing EPSPS copies. This suggests that genome instability imposes a constraint on the evolution of herbicide resistance through increased EPSPS copy number.