Abstract
Non-target site resistance (NTSR) to herbicides in black-grass (Alopecurus myosuroides) results in enhanced tolerance to multiple chemistries and is widespread in Northern Europe. To help define the underpinning mechanisms of resistance, global transcriptome and biochemical analysis have been used to phenotype three NTSR black-grass populations. These comprised NTSR1 black-grass from the classic Peldon field population, which shows broad-ranging resistance to post-emergence herbicides; NTSR2 derived from herbicide-sensitive (HS) plants repeatedly selected for tolerance to pendimethalin; and NTSR3 selected from HS plants for resistance to fenoxaprop-P-ethyl. NTSR in weeds is commonly associated with enhanced herbicide metabolism catalyzed by glutathione transferases (GSTs) and cytochromes P450 (CYPs). As such, the NTSR populations were assessed for their ability to detoxify chlorotoluron, which is detoxified by CYPs and fenoxaprop-P-ethyl, which is acted on by GSTs. As compared with HS plants, enhanced metabolism toward both herbicides was determined in the NTSR1 and NTSR2 populations. In contrast, the NTSR3 plants showed no increased detoxification capacity, demonstrating that resistance in this population was not due to enhanced metabolism. All resistant populations showed increased levels of AmGSTF1, a protein functionally linked to NTSR and enhanced herbicide metabolism. Enhanced AmGSTF1 was associated with increased levels of the associated transcripts in the NTSR1 and NTSR2 plants, but not in NTSR3, suggestive of both pre- and post-transcriptional regulation. The related HS, NTSR2, and NTSR3 plants were subject to global transcriptome sequencing and weighted gene co-expression network analysis to identify modules of genes with coupled regulatory functions. In the NTSR2 plants, modules linked to detoxification were identified, with many similarities to the transcriptome of NTSR1 black-grass. Critical detoxification genes included members of the CYP81A family and tau and phi class GSTs. The NTSR2 transcriptome also showed network similarities to other (a)biotic stresses of plants and multidrug resistance in humans. In contrast, completely different gene networks were activated in the NTSR3 plants, showing similarity to the responses to cold, osmotic shock and fungal infection determined in cereals. Our results demonstrate that NTSR in black-grass can arise from at least two distinct mechanisms, each involving complex changes in gene regulatory networks.
Highlights
Black-grass (Alopecurus myosuroides) is an annual grass weed of cereals that is widely dispersed in genetically diverse populations across Western Europe (Moss, 1979)
The NTSR3 plants were only resistant toward the acetyl-CoA carboxylase (ACCase) herbicide fenoxaprop-P-ethyl, while the NTSR2 population was resistant toward pendimethalin and ACCase inhibitors, but not to compounds acting on acetolactate synthase (ALS) (Tétard-Jones et al, 2018)
In the case of fenoxaprop, while more of the CBO-SG glutathione conjugate was determined in NTSR1 and NTSR2, the levels of parent fenoxaprop were equivalent to those determined in the HS plants, suggesting the herbicide was in some type of equilibrium between soluble and insoluble forms (Figures 2A,B)
Summary
Black-grass (Alopecurus myosuroides) is an annual grass weed of cereals that is widely dispersed in genetically diverse populations across Western Europe (Moss, 1979). Herbicide resistance is widespread in these populations; and in the United Kingdom, the respective loss of weed control incurs an economic cost of ∼0.5 bn GBP/year, being associated with 1 million ton/year of yield loss in wheat production (Varah et al, 2020). Within these resistant populations, non-target site resistance (NTSR) is commonly encountered and difficult to combat, as it contributes to loss of control of many pre- and postemergence selective herbicides, irrespective of their chemistry or mode of action (Preston, 2004). Central to EMR is the enhanced expression of proteins involved in herbicide detoxification, which includes cytochromes P450 (CYPs), glutathione transferases (GSTs), UDP-glycosyltransferases (UGTs), and ATP-binding cassette transporters (ABC transporters) These proteins act collectively to detoxify herbicides (Délye, 2013). In contrast to EMR, the molecular components of other NTSR mechanisms remain largely unknown
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