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

Edited by Ronald L. Phillips, University of Minnesota, St. Paul, MN, and approved February 15, 2018 (received for review November 6, 2017)
March 12, 2018
115 (13) 3332-3337

Significance

Glyphosate is a nonselective herbicide used around the globe for weed control in glyphosate-resistant (GR) and noncrop situations. The extensive and exclusive use of glyphosate has led to the evolution of herbicide resistance in many crop weeds. The molecular target of glyphosate, the 5-enolpyruvlyshikimate-3-phosphate synthase (EPSPS) gene, confers resistance upon amplification and was first documented in GR Amaranthus palmeri. We now report that amplified EPSPS copies in GR A. palmeri are present in the form of extrachromosomal circular DNA molecules (eccDNAs) with various conformations. We discovered that eccDNAs are transmitted to the next generation by tethering to mitotic and meiotic chromosomes. These results represent a report of extrachromosomal structures that drive rapid adaptive evolution in higher organisms.

Abstract

Gene amplification has been observed in many bacteria and eukaryotes as a 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 extrachromosomal elements that usually contain autonomously replicating extrachromosomal 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 an 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 [McClintock B (1978) Stadler Genetics Symposium] 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.

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Acknowledgments

We thank John Raupp for critical review of the manuscript and Duane Wilson for technical assistance. This research was supported by grants from the Kansas Wheat Commission and the Kansas Crop Improvement Association, Wheat Genetics Resource Center Industry/University Cooperative Research Center National Science Foundation Contract 1338897, and Department of Agronomy and US Department of Agriculture-Agricultural Research Services Project 6066-21000-060-00-D 9. This is contribution number 18-189-J from the Kansas Agricultural Experiment Station (Kansas State University).

Supporting Information

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Information & Authors

Information

Published in

Go to Proceedings of the National Academy of Sciences
Proceedings of the National Academy of Sciences
Vol. 115 | No. 13
March 27, 2018
PubMed: 29531028

Classifications

Submission history

Published online: March 12, 2018
Published in issue: March 27, 2018

Keywords

  1. 5-enolpyruvylshikimate-3-phosphate synthase
  2. eccDNA
  3. glyphosate resistance
  4. adaptive evolution
  5. gene amplification

Acknowledgments

We thank John Raupp for critical review of the manuscript and Duane Wilson for technical assistance. This research was supported by grants from the Kansas Wheat Commission and the Kansas Crop Improvement Association, Wheat Genetics Resource Center Industry/University Cooperative Research Center National Science Foundation Contract 1338897, and Department of Agronomy and US Department of Agriculture-Agricultural Research Services Project 6066-21000-060-00-D 9. This is contribution number 18-189-J from the Kansas Agricultural Experiment Station (Kansas State University).

Notes

This article is a PNAS Direct Submission.

Authors

Affiliations

Dal-Hoe Koo
Wheat Genetics Resource Center and Department of Plant Pathology, Kansas State University, Manhattan, KS 66506;
William T. Molin
Crop Production Systems Research Unit, US Department of Agriculture-Agricultural Research Services, Stoneville, MS 38776;
Christopher A. Saski
Institute for Translational Genomics, Clemson University, Clemson, SC 29634;
Jiming Jiang
Department of Plant Biology, Michigan State University, East Lansing, MI 48824;
Department of Horticulture, Michigan State University, East Lansing, MI 48824;
Karthik Putta
Department of Agronomy, Kansas State University, Manhattan, KS 66506
Department of Agronomy, Kansas State University, Manhattan, KS 66506
Bernd Friebe
Wheat Genetics Resource Center and Department of Plant Pathology, Kansas State University, Manhattan, KS 66506;
Bikram S. Gill1 [email protected]
Wheat Genetics Resource Center and Department of Plant Pathology, Kansas State University, Manhattan, KS 66506;

Notes

1
To whom correspondence may be addressed. Email: [email protected] or [email protected].
Author contributions: D.-H.K., W.T.M., C.A.S., J.J., M.J., B.F., and B.S.G. designed research; D.-H.K., W.T.M., C.A.S., K.P., M.J., B.F., and B.S.G. performed research; D.-H.K., W.T.M., C.A.S., J.J., M.J., B.F., and B.S.G. analyzed data; and D.-H.K., W.T.M., C.A.S., M.J., B.F., and B.S.G. wrote the paper.

Competing Interests

The authors declare no conflict of interest.

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    Extrachromosomal circular DNA-based amplification and transmission of herbicide resistance in crop weed Amaranthus palmeri
    Proceedings of the National Academy of Sciences
    • Vol. 115
    • No. 13
    • pp. 3193-E3068

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