Molecular Mechanisms of Herbicide Resistance in Weeds

A special issue of Genes (ISSN 2073-4425). This special issue belongs to the section "Plant Genetics and Genomics".

Deadline for manuscript submissions: closed (5 July 2022) | Viewed by 18549

Special Issue Editors

Agrotecnio Centre for Research, Universitat de Lleida, Avda. Rovira Roure 191, 25198 Lleida, Spain
Interests: herbicide resistance; resistant mechanisms; herbicides; enhanced metabolism; weeds; herbicide-degrading enzymes; cross-resistance

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Co-Guest Editor
Center for Advanced Research in Weed Science, Department of Plant Protection, School of Agriculture, São Paulo State University, Botucatu, SP, Brazil
Interests: herbicide cross resistance; herbicide multiple resistance; herbicides; weeds; CytP450; GST; resistant mechanisms
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Special Issue Information

Dear Colleagues,

The continued use of herbicides as a tool for weed control is being threatened by the steady increase of herbicide resistance. To ensure their sustained use in agriculture, there is great interest in understanding the molecular mechanisms conferring resistance or predisposing weeds toward evolving herbicide resistance.

Herbicide resistance is governed by target-site resistance (TSR) and non-target-site resistance (NTSR) mechanisms. TSR-based resistance is caused by gene alterations that induce amino acid substitution in encoded target enzyme, which modifies the structural conformation of this enzyme, leading to limited herbicide binding or enzyme expression. Resistance governed by TSR mechanisms is better understood because it is monogenic; however, NTSR mechanisms are rarely fully understood since they are quantitative in nature and controlled by several genes (with each gene providing some level of resistance); in other words, NTSR-based resistance is polygenic.

The increase in multiple resistance to different modes of action of herbicides due to NTSR-based resistance, mainly through enhanced metabolism, is of great concern. The arrival of next-generation sequencing (NGS) technologies has made tools and high-quality whole-genome sequences available for the first weeds. Furthermore, several methodologies have been developed for high-throughput phenotyping, which can be applied toward understanding gene expression regulation, or identifying single-nucleotide polymorphisms including RAD-Seq/GBS, or single-primer enrichment technology as well as amplicon-based NGS. These technologies should allow understanding of the evolutionary processes in herbicide resistance and the genetic basis of NTSR.

This Special Issue will focus on the new well-characterized cases of herbicide resistance, both for TSR and/or NTSR (if molecular basis is reported), and also on studies that identify new gene alterations conferring TSR or the genetic basis involved in NTSR. Submissions on herbicide resistance evolution as studied at the molecular level are also very welcome.

Dr. Joel Torra
Dr. Ricardo Alcántara-de la Cruz
Guest Editors

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Keywords

  • target site resistance (TSR)
  • non-target site resistance (NTSR)
  • enhanced metabolism
  • herbicide-degrading enzymes
  • cross-resistance
  • resistance evolution
  • next-generation sequencing (NGS)

Published Papers (7 papers)

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Editorial

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5 pages, 235 KiB  
Editorial
Molecular Mechanisms of Herbicide Resistance in Weeds
by Joel Torra and Ricardo Alcántara-de la Cruz
Genes 2022, 13(11), 2025; https://doi.org/10.3390/genes13112025 - 3 Nov 2022
Cited by 9 | Viewed by 2066
Abstract
Herbicides have become one of the most widespread weed-control tools in the world since their advent in the mid-20th century [...] Full article
(This article belongs to the Special Issue Molecular Mechanisms of Herbicide Resistance in Weeds)

Research

Jump to: Editorial

23 pages, 5175 KiB  
Article
Genome-Wide Evolutionary Analysis of Putative Non-Specific Herbicide Resistance Genes and Compilation of Core Promoters between Monocots and Dicots
by Saket Chandra and Ramon G. Leon
Genes 2022, 13(7), 1171; https://doi.org/10.3390/genes13071171 - 29 Jun 2022
Cited by 5 | Viewed by 2276
Abstract
Herbicides are key weed-control tools, but their repeated use across large areas has favored the evolution of herbicide resistance. Although target-site has been the most prevalent and studied type of resistance, non-target-site resistance (NTSR) is increasing. However, the genetic factors involved in NTSR [...] Read more.
Herbicides are key weed-control tools, but their repeated use across large areas has favored the evolution of herbicide resistance. Although target-site has been the most prevalent and studied type of resistance, non-target-site resistance (NTSR) is increasing. However, the genetic factors involved in NTSR are widely unknown. In this study, four gene groups encoding putative NTSR enzymes, namely, cytochrome-P450, glutathione-S-transferase (GST), uridine 5′-diphospho-glucuronosyltransferase (UDPGT), and nitronate monooxygenase (NMO) were analyzed. The monocot and dicot gene sequences were downloaded from publicly available databases. Phylogenetic trees revealed that most of the CYP450 resistance-related sequences belong to CYP81 (5), and in GST, most of the resistance sequences belonged to GSTU18 (9) and GSTF6 (8) groups. In addition, the study of upstream promoter sequences of these NTSR genes revealed stress-related cis-regulatory motifs, as well as eight transcription factor binding sites (TFBS) were identified. The discovered TFBS were commonly present in both monocots and dicots, and the identified motifs are known to play key roles in countering abiotic stress. Further, we predicted the 3D structure for the resistant CYP450 and GST protein and identified the substrate recognition site through the homology approach. Our description of putative NTSR enzymes may be used to develop innovative weed control techniques to delay the evolution of NTSR. Full article
(This article belongs to the Special Issue Molecular Mechanisms of Herbicide Resistance in Weeds)
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14 pages, 2414 KiB  
Article
Field-Evolved ΔG210-ppo2 from Palmer Amaranth Confers Pre-emergence Tolerance to PPO-Inhibitors in Rice and Arabidopsis
by Pamela Carvalho-Moore, Gulab Rangani, Ana Claudia Langaro, Vibha Srivastava, Aimone Porri, Steven J. Bowe, Jens Lerchl and Nilda Roma-Burgos
Genes 2022, 13(6), 1044; https://doi.org/10.3390/genes13061044 - 10 Jun 2022
Cited by 4 | Viewed by 2619
Abstract
Resistance to protoporphyrinogen IX oxidase (PPO)-inhibitors in Amaranthus palmeri and Amaranthus tuberculatus is mainly contributed by mutations in the PPO enzyme, which renders herbicide molecules ineffective. The deletion of glycine210 (ΔG210) is the most predominant PPO mutation. ΔG210-ppo2 is overexpressed in [...] Read more.
Resistance to protoporphyrinogen IX oxidase (PPO)-inhibitors in Amaranthus palmeri and Amaranthus tuberculatus is mainly contributed by mutations in the PPO enzyme, which renders herbicide molecules ineffective. The deletion of glycine210 (ΔG210) is the most predominant PPO mutation. ΔG210-ppo2 is overexpressed in rice (Oryza sativa c. ‘Nipponbare’) and Arabidopsis thaliana (Col-0). A foliar assay was conducted on transgenic T1 rice plants with 2× dose of fomesafen (780 g ha−1), showing less injury than the non-transgenic (WT) plants. A soil-based assay conducted with T2 rice seeds confirmed tolerance to fomesafen applied pre-emergence. In agar medium, root growth of WT rice seedlings was inhibited >90% at 5 µM fomesafen, while root growth of T2 seedlings was inhibited by 50% at 45 µM fomesafen. The presence and expression of the transgene were confirmed in the T2 rice survivors of soil-applied fomesafen. A soil-based assay was also conducted with transgenic A. thaliana expressing ΔG210-ppo2 which confirmed tolerance to the pre-emergence application of fomesafen and saflufenacil. The expression of A. palmeri ΔG210-ppo2 successfully conferred tolerance to soil-applied fomesafen in rice and Arabidopsis. This mutant also confers cross-tolerance to saflufenacil in Arabidopsis. This trait could be introduced into high-value crops that lack chemical options for weed management. Full article
(This article belongs to the Special Issue Molecular Mechanisms of Herbicide Resistance in Weeds)
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19 pages, 2871 KiB  
Article
High Resistance to Quinclorac in Multiple-Resistant Echinochloa colona Associated with Elevated Stress Tolerance Gene Expression and Enriched Xenobiotic Detoxification Pathway
by Gulab Rangani, Christopher E. Rouse, Christopher Saski, Rooksana E. Noorai, Vijay Shankar, Amy L. Lawton-Rauh, Isabel S. Werle and Nilda Roma-Burgos
Genes 2022, 13(3), 515; https://doi.org/10.3390/genes13030515 - 15 Mar 2022
Cited by 8 | Viewed by 2805
Abstract
Echinochloa colona and other species in this genus are a threat to global rice production and food security. Quinclorac, an auxin mimic, is a common herbicide for grass weed control in rice, and Echinochloa spp. have evolved resistance to it. The complete mode [...] Read more.
Echinochloa colona and other species in this genus are a threat to global rice production and food security. Quinclorac, an auxin mimic, is a common herbicide for grass weed control in rice, and Echinochloa spp. have evolved resistance to it. The complete mode of quinclorac action and subsequent evolution of resistance is not fully understood. We analyzed the de novo transcriptome of multiple-herbicide-resistant (ECO-R) and herbicide-susceptible genotypes in response to quinclorac. Several biological processes were constitutively upregulated in ECO-R, including carbon metabolism, photosynthesis, and ureide metabolism, indicating improved metabolic efficiency. The transcriptional change in ECO-R following quinclorac treatment indicates an efficient response, with upregulation of trehalose biosynthesis, which is also known for abiotic stress mitigation. Detoxification-related genes were induced in ECO-R, mainly the UDP-glycosyltransferase (UGT) family, most likely enhancing quinclorac metabolism. The transcriptome data also revealed that many antioxidant defense elements were uniquely elevated in ECO-R to protect against the auxin-mediated oxidative stress. We propose that upon quinclorac treatment, ECO-R detoxifies quinclorac utilizing UGT genes, which modify quinclorac using the sufficient supply of UDP-glucose from the elevated trehalose pathway. Thus, we present the first report of upregulation of trehalose synthesis and its association with the herbicide detoxification pathway as an adaptive mechanism to herbicide stress in Echinochloa, resulting in high resistance. Full article
(This article belongs to the Special Issue Molecular Mechanisms of Herbicide Resistance in Weeds)
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17 pages, 3951 KiB  
Article
Target-Site Mutations and Expression of ALS Gene Copies Vary According to Echinochloa Species
by Silvia Panozzo, Elisa Mascanzoni, Laura Scarabel, Andrea Milani, Giliardi Dalazen, Aldo J. Merotto, Patrick J. Tranel and Maurizio Sattin
Genes 2021, 12(11), 1841; https://doi.org/10.3390/genes12111841 - 22 Nov 2021
Cited by 17 | Viewed by 2228
Abstract
The sustainability of rice cropping systems is jeopardized by the large number and variety of populations of polyploid Echinochloa spp. resistant to ALS inhibitors. Better knowledge of the Echinochloa species present in Italian rice fields and the study of ALS genes involved in [...] Read more.
The sustainability of rice cropping systems is jeopardized by the large number and variety of populations of polyploid Echinochloa spp. resistant to ALS inhibitors. Better knowledge of the Echinochloa species present in Italian rice fields and the study of ALS genes involved in target-site resistance could significantly contribute to a better understanding of resistance evolution and management. Using a CAPS-rbcL molecular marker, two species, E. crus-galli (L.) P. Beauv. and E. oryzicola (Vasinger) Vasing., were identified as the most common species in rice in Italy. Mutations involved in ALS inhibitor resistance in the different species were identified and associated with the ALS homoeologs. The relative expression of the ALS gene copies was evaluated. Molecular characterization led to the identification of three ALS genes in E. crus-galli and two in E. oryzicola. The two species also carried different point mutations conferring resistance: Ala122Asn in E. crus-galli and Trp574Leu in E. oryzicola. Mutations were carried in the same gene copy (ALS1), which was significantly more expressed than the other copies (ALS2 and ALS3) in both species. These results explain the high resistance level of these populations and why mutations in the other ALS copies are not involved in herbicide resistance. Full article
(This article belongs to the Special Issue Molecular Mechanisms of Herbicide Resistance in Weeds)
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15 pages, 4608 KiB  
Article
Impact of a Novel W2027L Mutation and Non-Target Site Resistance on Acetyl-CoA Carboxylase-Inhibiting Herbicides in a French Lolium multiflorum Population
by Shiv Shankhar Kaundun, Joe Downes, Lucy Victoria Jackson, Sarah-Jane Hutchings and Eddie Mcindoe
Genes 2021, 12(11), 1838; https://doi.org/10.3390/genes12111838 - 21 Nov 2021
Cited by 6 | Viewed by 2436
Abstract
Herbicides that inhibit acetyl-CoA carboxylase (ACCase) are among the few remaining options for the post-emergence control of Lolium species in small grain cereal crops. Here, we determined the mechanism of resistance to ACCase herbicides in a Lolium multiflorum population (HGR) from France. A [...] Read more.
Herbicides that inhibit acetyl-CoA carboxylase (ACCase) are among the few remaining options for the post-emergence control of Lolium species in small grain cereal crops. Here, we determined the mechanism of resistance to ACCase herbicides in a Lolium multiflorum population (HGR) from France. A combined biological and molecular approach detected a novel W2027L ACCase mutation that affects aryloxyphenoxypropionate (FOP) but not cyclohexanedione (DIM) or phenylpyraxoline (DEN) subclasses of ACCase herbicides. Both the wild-type tryptophan and mutant leucine 2027-ACCase alleles could be positively detected in a single DNA-based-derived polymorphic amplified cleaved sequence (dPACS) assay that contained the targeted PCR product and a cocktail of two discriminating restriction enzymes. Additionally, we identified three well-characterised I1781L, I2041T, and D2078G ACCase target site resistance mutations as well as non-target site resistance in HGR. The non-target site component endowed high levels of resistance to FOP herbicides whilst partially impacting on the efficacy of pinoxaden and cycloxydim. This study adequately assessed the contribution of the W2027L mutation and non-target site mechanism in conferring resistance to ACCase herbicides in HGR. It also highlights the versatility and robustness of the dPACS method to simultaneously identify different resistance-causing alleles at a single ACCase codon. Full article
(This article belongs to the Special Issue Molecular Mechanisms of Herbicide Resistance in Weeds)
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12 pages, 2175 KiB  
Article
Understanding Resistance Mechanisms to Trifluralin in an Arkansas Palmer Amaranth Population
by Fidel González-Torralva and Jason K. Norsworthy
Genes 2021, 12(8), 1225; https://doi.org/10.3390/genes12081225 - 10 Aug 2021
Cited by 11 | Viewed by 2683
Abstract
Amaranthus palmeri S. Watson (Palmer amaranth) is considered a problematic and troublesome weed species in many crops in the USA, partly because of its ability to evolve resistance to herbicides. In this study, we explored the mechanism of resistance in a trifluralin-resistant A. [...] Read more.
Amaranthus palmeri S. Watson (Palmer amaranth) is considered a problematic and troublesome weed species in many crops in the USA, partly because of its ability to evolve resistance to herbicides. In this study, we explored the mechanism of resistance in a trifluralin-resistant A. palmeri accession collected from Arkansas, USA. Dose-response assays using agar plates demonstrated an EC50 (effective concentration that reduces root length by 50%) of 1.02 µM trifluralin compared to 0.39 µM obtained in the susceptible accession. Thus, under these conditions, the resistant accession required 2.6 times more trifluralin to inhibit root length by 50%. Seeds in the presence or absence of the cytochrome P450-inhibitior malathion displayed a differential response with no significant influence on root length, suggesting that resistance is not P450-mediated. In addition, application of 4-chloro-7-nitrobenzofurazan (NBD-Cl), a glutathione S-transferase (GST) inhibitor, showed significant differences in root length, indicating that GSTs are most likely involved in the resistance mechanism. Sequencing of α- and β-tubulin genes revealed no single nucleotide polymorphisms (SNPs) previously described between accessions. In addition, relative gene copy number of α- and β-tubulin genes were estimated; however, both resistant and susceptible accessions displayed similar gene copy numbers. Overall, our results revealed that GST-mediated metabolism contributes to trifluralin resistance in this A. palmeri accession from Arkansas. Full article
(This article belongs to the Special Issue Molecular Mechanisms of Herbicide Resistance in Weeds)
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