Analysis of multiple-herbicide resistant Amaranthus palmeri populations from Spain points to an introduction of the eccDNA from America
The herbicide-resistant invasive weed species Amaranthus palmeri threatens agricultural production and native plant ecology in Spain, as well as in other European countries. Understanding whether herbicide resistance alleles evolve in situ or are introduced via gene flow remains unclear. To address...
| Authors: | ; ; ; ; ; |
|---|---|
| Format: | Article |
| Publication date: | 2025 |
| Country: | España |
| Institution: | Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya) |
| Repository: | Recercat. Dipósit de la Recerca de Catalunya |
| OAI Identifier: | oai:recercat.cat:10459.1/468474 |
| Online Access: | https://doi.org/10.1002/ps.70034 https://hdl.handle.net/10459.1/468474 |
| Access Level: | Open access |
| Keyword: | ALS-resistance Extrachromosomal circular DNA Glyphosate-resistance |
| _version_ | 1878732797844127744 |
|---|---|
| author | Manicardi, Alfredo |
| author2 | Mora, Germán Araujo, André Lucas Simões Gaines, Todd A. Lozano-Juste, Jorge Torra Farré, Joel |
| author2_role | author author author author author |
| author_browse | Araujo, André Lucas Simões Gaines, Todd A. Lozano-Juste, Jorge Manicardi, Alfredo Mora, Germán Torra Farré, Joel |
| author_facet | Manicardi, Alfredo Mora, Germán Araujo, André Lucas Simões Gaines, Todd A. Lozano-Juste, Jorge Torra Farré, Joel |
| author_role | author |
| collection | Recercat. Dipósit de la Recerca de Catalunya |
| description | The herbicide-resistant invasive weed species Amaranthus palmeri threatens agricultural production and native plant ecology in Spain, as well as in other European countries. Understanding whether herbicide resistance alleles evolve in situ or are introduced via gene flow remains unclear. To address this, we characterized multiple resistance to acetolactate synthase (ALS)-- and 5-enolpyruvylshikimate-3phosphate synthase (EPSPS)-inhibiting herbicides in two Spanish A. palmeri populations at the plant level. Additionally, we analyzed the extra-chromosomal circular DNA (eccDNA) to determine whether glyphosate resistance resulted from local selection pressure or was introduced by gene flow. RESULTS: Both populations exhibit individuals that survived both herbicide MoA, with multiple resistance mechanisms to ALS- and EPSPS-inhibiting herbicides. Eight different ALS allele mutations were identified in resistant plants, including Pro-197-Ile, reported only in one species previously. Glyphosate resistance in the two populations is to the result of gene duplication mediated by eccDNA. Spanish and North American eccDNAs showed complete identity, with no single nucleotide polymorphisms (SNPs) found between the partial analyzed sequences of noncoding regions. CONCLUSION: We confirm for the first time in Europe resistance to ALS and EPSPS inhibitors at both the population and individual levels in two Spanish A. palmeri populations. The absence of SNPs in the eccDNA from Spanish populations compared to the reference American sequence and the presence of target-site mutations in the ALS gene occurred without selective pressure from ALS herbicides, suggests that the origin of resistance traits may have evolved elsewhere and been introduced from the place of origin to Spain. However, it is important to note that the limited number of populations studied and the partial sequencing of eccDNA do not provide definitive confirmation of the exact origins of resistance mechanisms. This work raises concerns about the arrival of this and potentially other new herbicide-resistant A. palmeri populations in Europe posing challenges for management. |
| eu_rights_str_mv | openAccess |
| format | article |
| id | ES_49f6e9d12b2e61ba3a490043577b65e9 |
| institution | Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya) |
| instname_str | Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya) |
| network_acronym_str | ES |
| network_name_str | España |
| oai_identifier_str | oai:recercat.cat:10459.1/468474 |
| publishDate | 2025 |
| publishDateSort | 2025 |
| publisher | John Wiley and Sons Ltd |
| publisherStr | John Wiley and Sons Ltd |
| reponame_str | Recercat. Dipósit de la Recerca de Catalunya |
| spelling | Analysis of multiple-herbicide resistant Amaranthus palmeri populations from Spain points to an introduction of the eccDNA from America Manicardi, Alfredo Mora, Germán Araujo, André Lucas Simões Gaines, Todd A. Lozano-Juste, Jorge Torra Farré, Joel ALS-resistance Extrachromosomal circular DNA Glyphosate-resistance The herbicide-resistant invasive weed species Amaranthus palmeri threatens agricultural production and native plant ecology in Spain, as well as in other European countries. Understanding whether herbicide resistance alleles evolve in situ or are introduced via gene flow remains unclear. To address this, we characterized multiple resistance to acetolactate synthase (ALS)-- and 5-enolpyruvylshikimate-3phosphate synthase (EPSPS)-inhibiting herbicides in two Spanish A. palmeri populations at the plant level. Additionally, we analyzed the extra-chromosomal circular DNA (eccDNA) to determine whether glyphosate resistance resulted from local selection pressure or was introduced by gene flow. RESULTS: Both populations exhibit individuals that survived both herbicide MoA, with multiple resistance mechanisms to ALS- and EPSPS-inhibiting herbicides. Eight different ALS allele mutations were identified in resistant plants, including Pro-197-Ile, reported only in one species previously. Glyphosate resistance in the two populations is to the result of gene duplication mediated by eccDNA. Spanish and North American eccDNAs showed complete identity, with no single nucleotide polymorphisms (SNPs) found between the partial analyzed sequences of noncoding regions. CONCLUSION: We confirm for the first time in Europe resistance to ALS and EPSPS inhibitors at both the population and individual levels in two Spanish A. palmeri populations. The absence of SNPs in the eccDNA from Spanish populations compared to the reference American sequence and the presence of target-site mutations in the ALS gene occurred without selective pressure from ALS herbicides, suggests that the origin of resistance traits may have evolved elsewhere and been introduced from the place of origin to Spain. However, it is important to note that the limited number of populations studied and the partial sequencing of eccDNA do not provide definitive confirmation of the exact origins of resistance mechanisms. This work raises concerns about the arrival of this and potentially other new herbicide-resistant A. palmeri populations in Europe posing challenges for management. We would like to acknowledge Maria Casamitjana Escobedo (University of Lleida) for providing technical support for plant growth. Her contributions were important to the completion of this study. This work has been supported by the Spanish State Research Agency, Spain (AEI) and the European Regional Development Fund, EU (ERDF) through the project PID2020\u2010113229RB\u2010C42. Joel Torra acknowledges support from the Spanish Ministry of Science, Innovation, and Universities. This project has received funding from the European Union's H2020 research and innovation program under Marie Sklodowska\u2010Curie grant agreement No 801586. Work at J.L\u2010J.'s group is funded by Spanish MCIN/AEI/PID2021\u2010128826OAI00, RYC2020\u2010029097\u2010I, (CISEJI/2022/26) grants and the AGROALNEXT program supported by MCIN with funding from European Union NextGenerationEU (PRTR\u2010C17.I1) and by Generalitat Valenciana. This work was conducted under the auspices of the research network PalmerNET funded by the Spanish Ministry of Science and Innovation (RED2022\u2010134285\u2010T). John Wiley and Sons Ltd https://doi.org/10.1002/ps.70034 https://hdl.handle.net/10459.1/468474 |
| spellingShingle | Analysis of multiple-herbicide resistant Amaranthus palmeri populations from Spain points to an introduction of the eccDNA from America Manicardi, Alfredo ALS-resistance Extrachromosomal circular DNA Glyphosate-resistance |
| title | Analysis of multiple-herbicide resistant Amaranthus palmeri populations from Spain points to an introduction of the eccDNA from America |
| title_full | Analysis of multiple-herbicide resistant Amaranthus palmeri populations from Spain points to an introduction of the eccDNA from America |
| title_fullStr | Analysis of multiple-herbicide resistant Amaranthus palmeri populations from Spain points to an introduction of the eccDNA from America |
| title_full_unstemmed | Analysis of multiple-herbicide resistant Amaranthus palmeri populations from Spain points to an introduction of the eccDNA from America |
| title_short | Analysis of multiple-herbicide resistant Amaranthus palmeri populations from Spain points to an introduction of the eccDNA from America |
| title_sort | Analysis of multiple-herbicide resistant Amaranthus palmeri populations from Spain points to an introduction of the eccDNA from America |
| topic | ALS-resistance Extrachromosomal circular DNA Glyphosate-resistance |
| topic_facet | ALS-resistance Extrachromosomal circular DNA Glyphosate-resistance |
| url | https://doi.org/10.1002/ps.70034 https://hdl.handle.net/10459.1/468474 |