Year: 2024
Type: article
Abstract: Herbicide resistance (HR) threatens global agriculture and food security with its increasing prevalence. HR evolves via two primary mechanisms: target site resistance (TSR), involving genetic mutations or duplications, and non-target-site resistance (NTSR), involving detoxification, uptake modification, or compartmentalization (Gaines et al., 2020; Box 1). Emerging evidence indicates that transposable elements (TEs) may also shape HR (Patterson et al., 2019; Cai et al., 2023). This viewpoint explores how TEs impact HR and its evolution. Although direct evidence remains limited, insights from studies on abiotic stress, where TEs are known to drive plant adaptation, may offer valuable evidence. Delving into these connections could open up new research avenues on plant evolution and transform strategies for managing HR. Diagramatic illustration of the molecular and biochemical mechanisms plants use to develop herbicide resistance. Mutations in herbicide target proteins prevent effective binding, while gene amplification boosts target protein expression, allowing plants to survive. Epigenetic modifications, such as DNA methylation, silence genes related to herbicide sensitivity or maintain genes promoting tolerance. Herbicide detoxification occurs in three phases: phase I modifies the herbicide (e.g. hydroxylation), phase II conjugates it with sugars, and phase III transports the detoxified molecules out of the cell. These processes enable resistant plants to survive and neutralize herbicides. Created in BioRender.com Evidence suggests that TEs and subtelomeric rearrangements drive glyphosate resistance in Eleusine indica (Zhang et al., 2023). The resistant genome (GR) harbours a 25-copy EPSPS (enolpyruvylshikimate-3-phosphate synthase) cassette, created via duplication and subtelomeric translocation, enhancing resistance by increasing gene dosage and repositioning. Gypsy retrotransposons, comprising 25% of the genome, cluster in subtelomeric regions, fuelling structural changes. Elevated recombination rates in GR subtelomeric regions facilitate unequal crossing over, driving rapid cassette proliferation and evolution of resistance (Zhang et al., 2023). TEs play a crucial role in the rapid evolution of HR in blackgrass (Alopecurus myosuroides). The blackgrass genome displays high heterozygosity, gene family expansion, and clusters of TEs, which contribute to its genomic plasticity. TEs near defence-related gene families, such as cytochrome P450 and GST genes, probably facilitate gene duplication, recombination, and regulatory changes, enabling rapid adaptation to herbicide pressure. TEs in regions enriched with key resistance-related quantitative trait loci (QTLs) and differentially expressed genes (DEGs) indicate that they help drive the parallel and non-parallel evolution of NTSR across different populations. Overall, TEs seem to be pivotal in enabling blackgrass to rapidly evolve and diversify its host resistance mechanisms (Cai et al., 2023). Glyphosate resistance in Kochia scoparia is conferred by an increased copy number of the EPSPS gene, with resistant populations typically harbouring 3–8 tandem EPSPS copies. Patterson et al. (2019) provide a draft genome assembly from a glyphosate-susceptible Kochia individual and a detailed assembly of the EPSPS locus from a glyphosate-resistant plant using bacterial artificial chromosome sequencing. A comparison of the resistant and susceptible loci revealed two dominant repeat types and highlighted several co-duplicated genes with altered transcription. Additionally, a mobile genetic element containing an FHY3/FAR1-like gene was discovered in the resistant line, associated with the EPSPS duplication. A model is proposed in which unequal crossing over, facilitated by this mobile element, drives EPSPS gene duplication and the evolution of glyphosate resistance. These findings enhance our understanding of the genetic mechanisms underlying rapid plant adaptation to stress (Patterson et al., 2019). Amaranthus palmeri exhibits rapid adaptation to herbicide pressure through dynamic genomic changes, with glyphosate resistance attributed to EPSPS gene amplification driven by TEs. Sequencing of resistant plants revealed DNA-mediated amplification of EPSPS copies, preserving intact introns alongside miniature inverted-repeat transposable elements (MITEs) co-located with the amplified genes. A putative Activator (Ac) transposase suggested TE-induced instability, enabling recombination or transposon-mediated replication. These findings indicate the pivotal role of TEs in driving resistance evolution, highlighting their contribution to genome plasticity under herbicide selection pressure (Gaines et al., 2013). HR crop varieties are vital for modern agriculture, enabling effective weed control without harming crops, and supporting sustainable farming to meet global food demands (Ofosu et al., 2023). TEs drive genetic variation in plant evolution by creating mutations, duplications, or regulatory changes, helping plants adapt to environmental challenges (Kirov, 2023). Unlike traditional breeding, which often relies on crossing and selecting for traits over multiple generations or introducing foreign DNA through genetic engineering, transposon-mediated breeding utilizes the inherent genomic machinery of plants to generate diversity. Despite its potential, this approach involves risks, as TE activity can result in unintended genomic disruptions or instability. TEs may contribute to adaptive HR by integrating into specific genomic regions and influencing gene regulation (Gressel, 2015). While direct evidence linking TEs to HR is limited, parallels from studies on insecticide resistance highlight their potential impact. For instance, in Drosophila melanogaster, the Accord TE insertion in the cytochrome P450 gene (Cyp6g1) promoter enhances detoxification, conferring DDT resistance and enabling its global spread (Daborn et al., 2002). However, resistance was also observed in lines without the Accord insertion, indicating the presence of additional mechanisms (Kuruganti et al., 2007). Similarly, in Helicoverpa zea, TEs were identified in the 5ʹ regions of xenobiotic-metabolizing genes, suggesting a role in regulating gene expression and adaptation. Moreover, in D. melanogaster, TEs associated with P450 genes linked to insecticide resistance were selectively retained near 5ʹ regions, emphasizing their functional role in environmental adaptation (Chen and Li, 2007). Exploring similar TE-mediated mechanisms in HR could offer valuable insights into adaptive resistance pathways in plants, aiding in mitigating critical challenges in sustainable agriculture. TEs can also influence the epigenetic landscape, modifying DNA methylation and histone structures to regulate gene expression dynamically in response to various abiotic stresses. Recent studies suggest that epigenetic mechanisms may play a crucial role in the evolution of HR (Pan et al., 2022). It can be hypothesized that under herbicide pressure, TEs could switch on the detoxification gene expression, enhancing resistance without causing permanent genomic changes. For example, in Arabidopsis thaliana, stress-induced mobilization of the ONSEN element preferentially targeted maternally expressed genes (MEGs) associated with H2A.Z and H3K27me3 marks. DNA hypomethylation further disrupted MEG imprinting, illustrating how stress-activated TE activity can drive lasting epigenetic changes that influence gene expression (Del Toro-De León et al., 2024). While this presents a potential parallel for HR, it remains a hypothesis to be tested. Experimental validation is essential to confirm that a transposon can detect herbicide stress, initiate epigenetic modifications that alter gene expression, and act swiftly enough to safeguard the plant against herbicide exposure, ensuring its survival. Furthermore, the heritability of these epigenetic changes must be established to fulfil the criteria for resistance. Transposons can also play a critical role in the evolution of resistance mechanisms by promoting the duplication of resistance-related genes. This phenomenon, well documented in bacteria (Maddamsetti et al., 2024) and insects (Heckel, 2022), highlights an evolutionarily conserved role for gene duplication in adapting to selective pressures. While HR through copy number variation (CNV) is less frequently observed than insecticide or antibiotic resistance, this discrepancy may partly stem from the challenges of detecting subtle CNVs in polyploid species. Extensive gene amplifications in species such as Amaranthus raise intriguing questions: could similar mechanisms operate in other plant species, or might adaptive deletions play a complementary role in refining resistance? Although the loss of essential genes rarely confers resistance, notable exceptions include clomazone resistance in cotton and triallate resistance in wild oats, which evolve more gradually due to their recessive nature (Kern et al., 1996). These insights highlight the diverse genetic pathways that plants can exploit to adapt to herbicide pressure. The evolutionary benefits of transposon-driven gene duplication must be weighed against the potential risks. Adaptive deletions within amplified regions could reduce fitness costs, but transposon activity also carries the potential to introduce lethal mutations or to destabilize the genome (Lisch, 2013). Furthermore, the ecological implications are profound, as horizontal gene transfer could spread resistance traits to weedy relatives. Retrotransposons have demonstrated the ability to cross species boundaries (Vrbničanin et al., 2017; Widen et al., 2023), raising concerns about transferring resistance traits into non-target species and complicating weed management. These evolutionary and ecological dynamics highlight the importance of vigilant monitoring and developing strategic interventions to mitigate the spread and impact of resistance traits in agricultural systems, ensuring sustainable farming practices and minimizing unintended consequences. Advances in genome-editing technologies such as CRISPR/Cas9 [clustered regularly interspaced palindromic repeats (CRISPR)/CRISPR-associated protein 9] have transformed transposons from random genomic elements into precise breeding tools. By targeting specific genes or regulatory sequences, breeders can induce mutations or gene duplications that enhance HR while minimizing unwanted genetic disruptions (Li et al., 2024; Liu et al., 2024). To validate these hypotheses, stress-inducing experiments could be conducted to observe TE activation in resistant versus susceptible plants under herbicide treatment. High-throughput sequencing methods such as RNA-seq [i.e. long- or short-read sequencing, single-cell transcriptomics] and ATAC-seq could monitor TE activation and associated changes in gene expression (Gandi et al., 2022). Additionally, CRISPR/Cas9-mediated activation or suppression of specific TEs can validate their functional roles, while epigenetic analyses using bisulfite sequencing or ChIP-seq can explore stress-induced regulatory changes near TEs. Artificial intelligence (AI) can further elevate this approach, with AI algorithms predicting optimal transposon insertion sites and machine learning simulating outcomes to optimize resistance traits (Orozco-Arias et al., 2019). However, challenges such as regulatory barriers, the complexity of simulating real-world agricultural conditions, and the scalability of CRISPR- and AI-based tools in developing countries must be addressed to ensure that these innovations translate effectively into practical applications. Nevertheless, these innovations, coupled with marker-assisted selection, can streamline the identification and propagation of beneficial traits, significantly accelerating the development of herbicide-resistant crops. Transposon tagging also offers a forward-looking avenue to disentangle new resistance pathways, expanding our understanding of genetic mechanisms driving plant evolution (Wu et al., 2023). Leveraging the potential of these cutting-edge tools offers more efficient, sustainable solutions for alleviating the challenges of modern agriculture. TEs are emerging as key drivers of herbicide resistance, enabling rapid adaptation through gene duplication, regulatory network rewiring, and stress response modifications. Advances such as CRISPR/Cas9 and AI algorithms potentially transform TEs from genomic risks into tools for precise genetic adaptation, holding great promise for sustainable crop improvement. Future research should focus on the crosstalk between TEs, detoxification pathways, and environmental stressors to expose novel mechanisms of resistance and resilience in crops. Box 2 highlights key questions that could drive future research directions. While deploying TEs for HR in crops is intriguing, they also offer unparalleled opportunities for innovation in crop breeding. However, multidisciplinary efforts are fundamental to harnessing the potential of TEs. How do transposons drive the evolution of multiherbicide resistance, and what genetic mechanisms are involved? Can transposon-induced gene disruption alter herbicide-targeted pathways, causing resistance beyond target site mutations? What molecular signatures from transposons could serve as biomarkers for early herbicide resistance detection? How do environmental stresses such as drought or salinity trigger transposon activation, affecting stress tolerance and herbicide resistance? Could transposon-induced epigenetic changes cause non-target site resistance, and are these changes stable across generations? What strategies can prevent transposon activation, and could this help in delaying the evolution of new resistance mechanisms? MKS and AR: conceptualization, writing, and designing the figures; MKS, KH, AR: and JS: review and editing; AR: English language proofreading; JS: funding acquisition. All authors edited and revised the final manuscript, contributed to the article, and approved the submitted version. No conflict of interest was declared. This work was supported by a grant from the National Agency of Agricultural Research, grant no. QL24010167 [The Ministry of Education, Youth and Sports (Czech Republic)]. AR acknowledges support from the ‘Excellent Team Grant’ from the Faculty of Forestry and Wood Sciences, CULS, Prague. Data are available from the corresponding author upon request.
Source: Journal of Experimental Botany
DOI: 10.1093/jxb/erae517
Institution: Czech University of Life Sciences Prague
Language: English
Subfield: Plant Science
Domain: Life Sciences
Open Access status: bronze
OpenAlex ID: W4405665295