The EccDNA Replicon: A heritable, extranuclear vehicle that enables gene amplification and glyphosate resistance in Amaranthus palmeri

Authors: Molin, William; YAGUCHI, ALLISON - Clemson University; BLENNER, MARK - Clemson University; SASKI, CHRISTOPHER - Clemson University

Submitted to: The Plant Cell
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/21/2020
Publication Date: 4/23/2020
Citation: Molin, W.T., Yaguchi, A., Blenner, M., Saski, C.A. 2020. The EccDNA Replicon: A Heritable, Extranuclear Vehicle That Enables Gene Amplification and Glyphosate Resistance in Amaranthus palmeri. The Plant Cell. 32:2132-2140. https://doi.org/10.1105/tpc.20.00099.
DOI: https://doi.org/10.1105/tpc.20.00099

Interpretive Summary: Palmer 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 size of the eccDNA and the genes contained within it. The results showed that the amplified unit conferring resistance was nearly four hundred kilobases long and had one hundred three genes. These results are important to farmers and society as a whole because it shows unanticipated changes in DNA content from over use of a herbicide.

Technical Abstract: Selective pressures in nature potentiate genomic plasticity as a mechanism of adaptation to sustain life. The predominant source of this functional diversity in eukaryotes and prokaryotes is gene copy number variation, which endows these adaptive processes. These unbalanced structural variations impart a considerable spectrum of phenotypic diversity. However, the underlying mechanisms that give rise to massive gene copy proliferation are poorly understood. Here, we show a unique result of genomic plasticity, the amplification of a massive extrachromosomal circular DNA (eccDNA) replicon, which is an extra-nuclear vehicle used by the Amaranthus palmeri genome to rapidly increase crucial gene copy numbers required for plant survival under extreme abiotic stress, the result of which confers resistance to the herbicide glyphosate. Upon exposure and continued selection with glyphosate, the A. palmeri genome has undergone extensive shuffling to form a plasmid-like structure, an eccDNA replicon, that harbors the EPSPS synthase gene and other encoded machinery whose functions traverse detoxification, replication, recombination, and membrane transport. The eccDNA replicon can exist in the extranuclear space and may replicate autonomously to function as a vehicle for gene amplification. Furthermore, the eccDNA replicon is comprised of a complex arrangement of repeat sequences and mobile genetic elements interspersed among arrays of clustered palindromes that may function in stability, DNA duplication, and/or a means of nuclear integration of the adjacent and intervening sequences. We anticipate that the discovery of the eccDNA replicon will elicit new approaches in understanding genome dynamics and evolutionary mechanisms. This structure has been engineered by nature to fulfill a unique biological role of providing genomic plasticity and to drive adaptive evolution and also holds potential to ignite a revolution in biotechnology and plant breeding via a new vehicle for DNA amplification and genome engineering.