Sequence Characterization of Extra-Chromosomal Circular DNA Content in Multiple Blackgrass (<i>Alopecurus myosuroides</i>) Populations
<i>Alopecurus myosuroides</i> (blackgrass) is a problematic weed of Western European winter wheat, and its success is largely due to widespread multiple-herbicide resistance. Previous analysis of F2 seed families derived from two distinct blackgrass populations exhibiting equivalent non-...
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MDPI AG
2023-10-01
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| Series: | Genes |
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| Online Access: | https://www.mdpi.com/2073-4425/14/10/1905 |
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| author | Wangfang Fu Dana R. MacGregor David Comont Christopher A. Saski |
| author_facet | Wangfang Fu Dana R. MacGregor David Comont Christopher A. Saski |
| author_sort | Wangfang Fu |
| collection | DOAJ |
| description | <i>Alopecurus myosuroides</i> (blackgrass) is a problematic weed of Western European winter wheat, and its success is largely due to widespread multiple-herbicide resistance. Previous analysis of F2 seed families derived from two distinct blackgrass populations exhibiting equivalent non-target site resistance (NTSR) phenotypes shows resistance is polygenic and evolves from standing genetic variation. Using a CIDER-seq pipeline, we show that herbicide-resistant (HR) and herbicide-sensitive (HS) F3 plants from these F2 seed families as well as the parent populations they were derived from carry extra-chromosomal circular DNA (eccDNA). We identify the similarities and differences in the coding structures within and between resistant and sensitive populations. Although the numbers and size of detected eccDNAs varied between the populations, comparisons between the HR and HS blackgrass populations identified shared and unique coding content, predicted genes, and functional protein domains. These include genes related to herbicide detoxification such as Cytochrome P450s, ATP-binding cassette transporters, and glutathione transferases including <i>AmGSTF1</i>. eccDNA content was mapped to the <i>A. myosuroides</i> reference genome, revealing genomic regions at the distal end of chromosome 5 and the near center of chromosomes 1 and 7 as regions with a high number of mapped eccDNA gene density. Mapping to 15 known herbicide-resistant QTL regions showed that the eccDNA coding sequences matched twelve, with four QTL matching HS coding sequences; only one region contained HR coding sequences. These findings establish that, like other pernicious weeds, blackgrass has eccDNAs that contain homologs of chromosomal genes, and these may contribute genetic heterogeneity and evolutionary innovation to rapidly adapt to abiotic stresses, including herbicide treatment. |
| first_indexed | 2024-03-11T10:15:02Z |
| format | Article |
| id | doaj.art-af5288051492446ba1d9def67db4797e |
| institution | Directory Open Access Journal |
| issn | 2073-4425 |
| language | English |
| last_indexed | 2024-03-11T10:15:02Z |
| publishDate | 2023-10-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Genes |
| spelling | doaj.art-af5288051492446ba1d9def67db4797e2023-11-16T10:29:44ZengMDPI AGGenes2073-44252023-10-011410190510.3390/genes14101905Sequence Characterization of Extra-Chromosomal Circular DNA Content in Multiple Blackgrass (<i>Alopecurus myosuroides</i>) PopulationsWangfang Fu0Dana R. MacGregor1David Comont2Christopher A. Saski3Department of Plant and Environmental Sciences, Clemson University, Clemson, SC 29634, USARothamsted Research, Protecting Crops and the Environment, Harpenden, Hertfordshire AL5 2JQ, UKRothamsted Research, Protecting Crops and the Environment, Harpenden, Hertfordshire AL5 2JQ, UKDepartment of Plant and Environmental Sciences, Clemson University, Clemson, SC 29634, USA<i>Alopecurus myosuroides</i> (blackgrass) is a problematic weed of Western European winter wheat, and its success is largely due to widespread multiple-herbicide resistance. Previous analysis of F2 seed families derived from two distinct blackgrass populations exhibiting equivalent non-target site resistance (NTSR) phenotypes shows resistance is polygenic and evolves from standing genetic variation. Using a CIDER-seq pipeline, we show that herbicide-resistant (HR) and herbicide-sensitive (HS) F3 plants from these F2 seed families as well as the parent populations they were derived from carry extra-chromosomal circular DNA (eccDNA). We identify the similarities and differences in the coding structures within and between resistant and sensitive populations. Although the numbers and size of detected eccDNAs varied between the populations, comparisons between the HR and HS blackgrass populations identified shared and unique coding content, predicted genes, and functional protein domains. These include genes related to herbicide detoxification such as Cytochrome P450s, ATP-binding cassette transporters, and glutathione transferases including <i>AmGSTF1</i>. eccDNA content was mapped to the <i>A. myosuroides</i> reference genome, revealing genomic regions at the distal end of chromosome 5 and the near center of chromosomes 1 and 7 as regions with a high number of mapped eccDNA gene density. Mapping to 15 known herbicide-resistant QTL regions showed that the eccDNA coding sequences matched twelve, with four QTL matching HS coding sequences; only one region contained HR coding sequences. These findings establish that, like other pernicious weeds, blackgrass has eccDNAs that contain homologs of chromosomal genes, and these may contribute genetic heterogeneity and evolutionary innovation to rapidly adapt to abiotic stresses, including herbicide treatment.https://www.mdpi.com/2073-4425/14/10/1905eccDNAblackgrassherbicide resistancerapid adaptation |
| spellingShingle | Wangfang Fu Dana R. MacGregor David Comont Christopher A. Saski Sequence Characterization of Extra-Chromosomal Circular DNA Content in Multiple Blackgrass (<i>Alopecurus myosuroides</i>) Populations Genes eccDNA blackgrass herbicide resistance rapid adaptation |
| title | Sequence Characterization of Extra-Chromosomal Circular DNA Content in Multiple Blackgrass (<i>Alopecurus myosuroides</i>) Populations |
| title_full | Sequence Characterization of Extra-Chromosomal Circular DNA Content in Multiple Blackgrass (<i>Alopecurus myosuroides</i>) Populations |
| title_fullStr | Sequence Characterization of Extra-Chromosomal Circular DNA Content in Multiple Blackgrass (<i>Alopecurus myosuroides</i>) Populations |
| title_full_unstemmed | Sequence Characterization of Extra-Chromosomal Circular DNA Content in Multiple Blackgrass (<i>Alopecurus myosuroides</i>) Populations |
| title_short | Sequence Characterization of Extra-Chromosomal Circular DNA Content in Multiple Blackgrass (<i>Alopecurus myosuroides</i>) Populations |
| title_sort | sequence characterization of extra chromosomal circular dna content in multiple blackgrass i alopecurus myosuroides i populations |
| topic | eccDNA blackgrass herbicide resistance rapid adaptation |
| url | https://www.mdpi.com/2073-4425/14/10/1905 |
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