The eccDNA mediated spread and rapid evolution of herbicide resistance in pigweed interspecific hybrids

Abstract

Extrachromosomal circular DNAs (eccDNAs) are found in many eukaryotic organisms. The eccDNA-powered copy number variation plays diverse roles from oncogenesis in humans to herbicide resistance in crop weeds. Here we report interspecific eccDNA flow and its dynamic behavior in soma cells of natural populations and F1 hybrids of Amaranthus sp. The glyphosate resistance (GR) trait is controlled by eccDNA-based amplification harboring the 5-enolpyruvylshikimate-3-phosphate synthase (EPSPS) gene (EPSPS-eccDNA), the molecular target of glyphosate. We documented pollen-mediated transfer of eccDNA in experimental hybrids between GS A. tuberculatus x GR A. palmeri. Experimental hybridization and fluorescence in situ hybridization (FISH) analysis revealed that the EPSPS-eccDNA present in A. spinosus was derived from GR A. palmeri by natural hybridization. FISH analysis also revealed random chromosome anchoring and massive EPSPS-eccDNA copy number variation in soma cells of weedy hybrids. The results suggest that eccDNAs are inheritable across compatible species contributing to genome plasticity and rapid adaptive evolution.