Extrachromosomal circular DNA-based amplification and transmission of herbicide resistance in crop weed Amaranthus palmeri

Authors: KOO, DAL-HOE - Kansas State University; Molin, William; SASKI, CHRISTOPHER - Clemson University; JIANG, JIMING - Michigan State University; PUTTA, KARTHIK - Kansas State University; JUGULAM, MITHILA - Clemson University; FRIEBE, BERND - Kansas State University; GILL, BIKRAM - Kansas State University

Submitted to: Proceedings of the National Academy of Sciences (PNAS)
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/15/2018
Publication Date: 3/1/2018
Citation: Koo, D., Molin, W.T., Saski, C.A., Jiang, J., Putta, K., Jugulam, M., Friebe, B., Gill, B.S. 2018. Extrachromosomal circular DNA-based amplification and transmission of herbicide resistance in crop weed Amaranthus palmeri. Proceedings of the National Academy of Sciences. hppts://doi.10.1073/pnas.1719354115.

Interpretive Summary: Pigweed (Amaranthus palmeri) with resistance to the herbicide glyphosate has been found across the United States and in each case the resistance was due to amplification of the target site on massive extrachromosomal circular deoxyribonucleic acid (eccDNA). Scientists in the USDA-ARS Crop Production Systems Research Unit, Stoneville, MS, Kansas State University and Clemson University conducted research to determine the morphology and size of the eccDNA. The results showed that the eccDNA was circular and tethered to chromosomes, and had one or more complete amplified units each of 399 kilobases in length. These results are important to farmers and the Weed Science Society as a whole because it shows unanticipated changes in DNA content from over use of a herbicide.

Technical Abstract: Gene amplification has been observed in many bacteria and eukaryotes as response to various selective pressures such as antibiotics, cytotoxic drugs, pesticides, herbicides and other stressful environmental conditions. An increase in gene copy number is often found as extra-chromosomal elements that usually contain autonomously replicating circular DNA molecules (eccDNAs). Amaranthus palmeri, a crop weed, can develop herbicide resistance to glyphosate [N-(phosphonomethyl) glycine] by amplification of the 5-enolpyruvylshikimate-3-phosphate synthase (EPSPS) gene, the molecular target of glyphosate. However, biological questions regarding the source of the amplified EPSPS, the nature of the amplified DNA structures, and mechanisms responsible for maintaining this gene amplification in cells and their inheritance, remain unknown. Here we report that amplified EPSPS copies in glyphosate-resistant (GR) A. palmeri are present in the form of eccDNAs with various conformations. The eccDNAs are transmitted during cell division in mitosis and meiosis to the soma and germ cells and the progeny by as yet unknown mechanism of tethering to mitotic and meiotic chromosomes. We propose that eccDNAs are one of the components of McClintock’s postulated innate systems that can rapidly produce soma variation, amplify EPSPS genes in the sporophyte that are transmitted to germ cells and modulate rapid glyphosate resistance through genome plasticity and adaptive evolution.