Pollen-mediated gene flow from glyphosate-resistant common waterhemp (Amaranthus rudis Sauer): consequences for the dispersal of resistance genes

Andrew J Tyre,Stevan Z Knezevic,Suat Irmak,John L Lindquist,Amit J Jhala,Todd A Gaines,Eric L Patterson,Debalin Sarangi

doi:10.1038/srep44913

Andrew J Tyre, Stevan Z Knezevic + Show 6 more

Open Access

https://doi.org/10.1038/srep44913

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Abstract

Gene flow is an important component in evolutionary biology; however, the role of gene flow in dispersal of herbicide-resistant alleles among weed populations is poorly understood. Field experiments were conducted at the University of Nebraska-Lincoln to quantify pollen-mediated gene flow (PMGF) from glyphosate-resistant (GR) to -susceptible (GS) common waterhemp using a concentric donor-receptor design. More than 130,000 common waterhemp plants were screened and 26,199 plants were confirmed resistant to glyphosate. Frequency of gene flow from all distances, directions, and years was estimated with a double exponential decay model using Generalized Nonlinear Model (package gnm) in R. PMGF declined by 50% at <3 m distance from the pollen source, whereas 90% reduction was found at 88 m (maximum) depending on the direction of the pollen-receptor blocks. Amplification of the target site gene, 5-enolpyruvylshikimate-3-phosphate synthase (EPSPS), was identified as the mechanism of glyphosate resistance in parent biotype. The EPSPS gene amplification was heritable in common waterhemp and can be transferred via PMGF, and also correlated with glyphosate resistance in pseudo-F2 progeny. This is the first report of PMGF in GR common waterhemp and the results are critical in explaining the rapid dispersal of GR common waterhemp in Midwestern United States.

Highlights

Gene flow refers to both the movement and introduction of genes and gene complexes into ‘allochthonous gene pools’[1]
enolpyruvylshikimate-3-phosphate synthase (EPSPS) gene amplification was reported in a GR biotype of Palmer amaranth collected from Georgia, but fluorescence in situ hybridization (FISH) analysis suggested that the amplified genes were dispersed throughout the genome[41]
It was believed that the common waterhemp plants in both the pollen-donor block and the closer distances were growing in a higher density compared to the plants at the farthest distances, causing a brief gap (

Summary

Introduction

Gene flow refers to both the movement and introduction of genes and gene complexes into ‘allochthonous (distant) gene pools’[1]. Spatial restrictions on gene dispersal lead to non-random mating that can result in the transformation of a population-subdivision into genetic neighborhoods, whereas extensive gene flow at the landscape scale promotes homogeneity among plant populations[5,6]. Its dioecy and anemophilous nature are believed to promote the rapid spread of the herbicide-resistant alleles in an agricultural landscape via pollen migration[32]. An overproduction of the enzyme EPSPS (5-enolpyruvylshikimate-3-phosphate synthase, the biological target of herbicide glyphosate) through additional EPSPS gene copies was responsible for glyphosate resistance in common waterhemp biotypes collected from several Midwestern states[38,39]. EPSPS gene amplification was reported in a GR biotype of Palmer amaranth collected from Georgia, but fluorescence in situ hybridization (FISH) analysis suggested that the amplified genes were dispersed throughout the genome[41]

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