Extrachromosomal circular DNA-based amplification and transmission of herbicide resistance in crop weed Amaranthus palmeri
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 t...
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description | 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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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.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.1719354115</identifier><identifier>PMID: 29531028</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>3-Phosphoshikimate 1-Carboxyvinyltransferase - genetics ; Amaranthus - drug effects ; Amaranthus - enzymology ; Amaranthus - genetics ; Amaranthus palmeri ; Amplification ; Antibiotics ; Biological Sciences ; Cell division ; Chromosomes ; Chromosomes, Plant ; Circular DNA ; Copy number ; Crops ; Cytotoxicity ; Deoxyribonucleic acid ; DNA ; DNA, Circular ; Environmental conditions ; Eukaryotes ; Gene Amplification ; Gene Expression Regulation, Plant ; Genetics ; Genomes ; Germ cells ; Glycine ; Glycine - analogs & derivatives ; Glycine - pharmacology ; Glyphosate ; Herbicide resistance ; Herbicide Resistance - genetics ; Herbicides ; Herbicides - pharmacology ; Heredity ; Meiosis ; Mitosis ; Pesticides ; Plant resistance ; Progeny ; Replicating ; Tethering ; Weeds</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2018-03, Vol.115 (13), p.3332-3337</ispartof><rights>Volumes 1–89 and 106–114, copyright as a collective work only; author(s) retains copyright to individual articles</rights><rights>Copyright © 2018 the Author(s). Published by PNAS.</rights><rights>Copyright National Academy of Sciences Mar 27, 2018</rights><rights>Copyright © 2018 the Author(s). Published by PNAS. 2018</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c489t-e54cbe214dfcbce43b3c70e06493513fb142ea7578a5ec8f5480e624721b2893</citedby><cites>FETCH-LOGICAL-c489t-e54cbe214dfcbce43b3c70e06493513fb142ea7578a5ec8f5480e624721b2893</cites><orcidid>0000-0003-2065-9067</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/26508227$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/26508227$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,727,780,784,803,885,27924,27925,53791,53793,58017,58250</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/29531028$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Koo, Dal-Hoe</creatorcontrib><creatorcontrib>Molin, William T.</creatorcontrib><creatorcontrib>Saski, Christopher A.</creatorcontrib><creatorcontrib>Jiang, Jiming</creatorcontrib><creatorcontrib>Putta, Karthik</creatorcontrib><creatorcontrib>Jugulam, Mithila</creatorcontrib><creatorcontrib>Friebe, Bernd</creatorcontrib><creatorcontrib>Gill, Bikram S.</creatorcontrib><title>Extrachromosomal circular DNA-based amplification and transmission of herbicide resistance in crop weed Amaranthus palmeri</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>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.</description><subject>3-Phosphoshikimate 1-Carboxyvinyltransferase - genetics</subject><subject>Amaranthus - drug effects</subject><subject>Amaranthus - enzymology</subject><subject>Amaranthus - genetics</subject><subject>Amaranthus palmeri</subject><subject>Amplification</subject><subject>Antibiotics</subject><subject>Biological Sciences</subject><subject>Cell division</subject><subject>Chromosomes</subject><subject>Chromosomes, Plant</subject><subject>Circular DNA</subject><subject>Copy number</subject><subject>Crops</subject><subject>Cytotoxicity</subject><subject>Deoxyribonucleic acid</subject><subject>DNA</subject><subject>DNA, Circular</subject><subject>Environmental conditions</subject><subject>Eukaryotes</subject><subject>Gene Amplification</subject><subject>Gene Expression Regulation, Plant</subject><subject>Genetics</subject><subject>Genomes</subject><subject>Germ cells</subject><subject>Glycine</subject><subject>Glycine - analogs & derivatives</subject><subject>Glycine - pharmacology</subject><subject>Glyphosate</subject><subject>Herbicide resistance</subject><subject>Herbicide Resistance - genetics</subject><subject>Herbicides</subject><subject>Herbicides - pharmacology</subject><subject>Heredity</subject><subject>Meiosis</subject><subject>Mitosis</subject><subject>Pesticides</subject><subject>Plant resistance</subject><subject>Progeny</subject><subject>Replicating</subject><subject>Tethering</subject><subject>Weeds</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpVkUtv1DAUhS0EokNhzQpkiXVaXz_G9gZpVMpDqmDTveU4N4xHSRzshNevx6MpLaws3fud43N1CHkJ7AKYFpfz5MsFaLBCSQD1iGyAWWi20rLHZMMY142RXJ6RZ6UcGGNWGfaUnHGrBDBuNuT39c8l-7DPaUwljX6gIeawDj7Td593TesLdtSP8xD7GPwS00T91NGqmcoYSzkOUk_3mNsYYoc0Y4ll8VNAGicacprpD6weu9FXzbJfC539MGKOz8mT3g8FX9y95-T2_fXt1cfm5suHT1e7myZIY5cGlQwtcpBdH9qAUrQiaIas3igUiL4FydFrpY1XGEyvpGG45VJzaLmx4py8PdnOaztiF3Cq4Qc351gT_XLJR_f_Zop79zV9d8pou7VQDd7cGeT0bcWyuENa81QjOw4MhACjjtTliaonl5Kxv_8BmDt25Y5duYeuquL1v8Hu-b_lVODVCTiUJeWH_VYxw7kWfwCG_Z0m</recordid><startdate>20180327</startdate><enddate>20180327</enddate><creator>Koo, Dal-Hoe</creator><creator>Molin, William T.</creator><creator>Saski, Christopher A.</creator><creator>Jiang, Jiming</creator><creator>Putta, Karthik</creator><creator>Jugulam, Mithila</creator><creator>Friebe, Bernd</creator><creator>Gill, Bikram S.</creator><general>National Academy of Sciences</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-2065-9067</orcidid></search><sort><creationdate>20180327</creationdate><title>Extrachromosomal circular DNA-based amplification and transmission of herbicide resistance in crop weed Amaranthus palmeri</title><author>Koo, Dal-Hoe ; 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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.</abstract><cop>United States</cop><pub>National Academy of Sciences</pub><pmid>29531028</pmid><doi>10.1073/pnas.1719354115</doi><tpages>6</tpages><orcidid>https://orcid.org/0000-0003-2065-9067</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | 3-Phosphoshikimate 1-Carboxyvinyltransferase - genetics Amaranthus - drug effects Amaranthus - enzymology Amaranthus - genetics Amaranthus palmeri Amplification Antibiotics Biological Sciences Cell division Chromosomes Chromosomes, Plant Circular DNA Copy number Crops Cytotoxicity Deoxyribonucleic acid DNA DNA, Circular Environmental conditions Eukaryotes Gene Amplification Gene Expression Regulation, Plant Genetics Genomes Germ cells Glycine Glycine - analogs & derivatives Glycine - pharmacology Glyphosate Herbicide resistance Herbicide Resistance - genetics Herbicides Herbicides - pharmacology Heredity Meiosis Mitosis Pesticides Plant resistance Progeny Replicating Tethering Weeds |
title | Extrachromosomal circular DNA-based amplification and transmission of herbicide resistance in crop weed Amaranthus palmeri |
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