Open access peer-reviewed chapter

New Insight in Herbicides Science: Non-Target Site Resistance and Its Mechanisms

Written By

Ermias Misganaw Amare

Submitted: 20 April 2022 Reviewed: 05 May 2022 Published: 01 February 2023

DOI: 10.5772/intechopen.105173

From the Edited Volume

New Insights in Herbicide Science

Edited by Kassio Ferreira Mendes

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Abstract

Managing weeds in crop production, whether in the field, or greenhouse, can be troublesome; however, it is essential to successful production. Weeds compete with the crop for nutrients, space, sunlight and also host plant pathogens and insect pests. The economic impacts of weeds include both monetary and non-monetary. In Australia, the overall cost of weeds to grain growers is estimated at AUD 3.3 billion annually. In India, weeds cost over USD 11 billion each year. In the USA, weeds cost USD 33 billion in lost crop production annually. Herbicide use is indispensable in agriculture as it offers tool for weed management; however, repeated applications of herbicides with the same mode of action resulted in the selection of herbicide-resistant weed populations. Herbicide resistance is a rapidly growing worldwide problem that causes significant crop yield losses as well as increases in production costs. Non-target-site resistance to herbicides in weeds can be conferred as a result of the alteration of one or more physiological processes such as reduced herbicide translocation, increased herbicide metabolism, decreased rate of herbicide activation. Non-Target Site Resistance mechanisms are generally more complex and can impart cross-resistance to herbicides with different modes of action. To date, approximately 252 species have evolved resistance to 23 of the 26 known herbicide modes of action.

Keywords

  • non-target site resistance
  • absorption
  • translocation
  • metabolism

1. Introduction

Weed is one of the main biotic factors that brings about a significant crop yield loss since the beginning of agriculture about 10,000 years ago. Weed will cause the highest potential yield loss to crops. In addition, weeds harbor insects pests, and pathogens, which attack crop plants. Weeds compete with crops for sunlight, water, nutrients, and space. Moreover, weeds infest and destroy native habitats, threatening native plants and grazing lands. Crop yield losses as a result of weeds depend on several factors including weed emergence time, weed density, type of weeds, type of crops, soil fertility, etc. Left uncontrolled, weeds can result in 100% yield loss. In Australia, the overall cost of weeds to grain growers is estimated at AUD 3.3 billion annually. In terms of yield losses, weed loss amounted to 2.7 million tons of grain at a national level [1]. In India, weeds cost over USD 11 billion each year [2]. In India, the yield losses because of weeds were estimated at 36% in peanut, 31% in soybean, 25% in maize, and 19% in wheat. In the USA, weeds cost USD 33 billion in lost crop production annually [2]. Hence, weed management is one of the most important components of cropping systems, which results in significant yield loss as well as increased cost of production. In the early 1950s, synthetic herbicides revolutionized agriculture and have been at the foundation of both weed science research and the intensification and expansion of industrialized agriculture [3].

In developing countries, where farm size is small, weeds management is carried out by hand removal however as a result of rising labor costs and it is being replaced by herbicide use. In most developed countries, herbicides are already widely used to control weeds. However, repeated application of herbicides with similar modes of action has resulted in the development of herbicide-resistant weeds. Currently, more than 500 unique cases of herbicide-resistant weeds have been documented across the globe [4]. The majority of herbicide-resistance weed cases were reported from the USA (more than 160) followed by Australia (over 90 cases) and the remaining cases are reported from Canada, China, and Brazil. The maximum number of herbicide-resistant weed species was reported in different crops, including wheat, maize, rice, soybean spring barley, canola, and cotton [4]. These crops are the most widely produced food crops as well as the important industrial crops. Glyphosate is the most traded herbicide across the globe and used for non-selective post-emergence control of both annual and perennial weeds [3]. This herbicide disrupts the activity of enzymes including 5-enolypyruvyshikimate-3-phospahate synthase [5, 6].

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2. Weed management methods

Managing weeds in crop production, whether in the field, greenhouses, or outdoor containers, can be troublesome; however, it is essential to successful production. Weeds not only compete with the crop for plant nutrients, space, and sunlight but also serve as an alternative host to virulent plant pathogens and notorious insect pests. The economic impacts of weeds include both monetary and non-monetary. For example, blackberries restrict human and animal access, harbor pests, reduce pasture production, impede establishment of plants, and reduce naturalness and biodiversity [7]. Some of the common weed management practices are explained below. Weed management activities include preventive/ quarantine, use of cover crops, mowing, flaming, mulching, solarization, and herbicide application.

2.1 Herbicides

In modern agriculture, herbicide spray are very common and rapid weed management method in many crop production areas across the globe. By using herbicides before weeds emerge, weed competition with the crop can be reduced or eliminated, resulting in higher yield and fewer labor costs despite ecological disturbance and health hazards. Herbicides are generally classified according to time of application to the crops and weed growth stage. Preplant herbicides are applied before planting. These herbicides are used before the desirable plants are present because some can control both germinating seedlings and established plants. Pre-emergence herbicides kill weeds at the seed germination stage. These herbicides are applied before weeds emerge. Post-emergence herbicides are applied after the weeds have emerged. Pre-emergence and post-emergence herbicides may be applied before or after the crop is planted depending on the crop and the herbicide selected. However, their extensive utilization across the globe imposes strong selection pressure on resistant weed populations, threatening our ability to successfully manage weed populations. Herbicide resistance is a rapidly growing worldwide problem that causes significant crop yield and quality losses as well as increases production costs. To date, approximately 252 species have evolved resistance to 23 of the 26 known herbicide modes of action, representing over 161 different herbicides [8].

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3. Herbicide resistance

The acquired inheritable trait of plants to survive and reproduce under herbicide exposure is defined as resistance. The Weed Science Society of America defines herbicide resistance as the inherited ability of a plant to survive and reproduce following exposure to a dose of herbicide normally lethal to the wild type. Under continuous selection pressure, that is, the repeated use of herbicides with the same mode of action, the resistant weed plants increase in frequency over time, resulting in the domination by individuals resistant to a particular herbicide. Biological and genetic factors of weed species, properties of herbicides, and agronomic practices play a significant role in the evolution and spread of herbicide resistance [8]. Biological characteristics of troublesome weeds, including prolific seed production, high germination percentage, seed dispersal, and longevity, help to maintain a high frequency of resistant individuals in the population. Genetic factors, such as natural mutations conferring herbicide resistance, inheritance of herbicide-resistant genes in the weed population, and fitness of resistance genes in the presence or absence of the herbicide, also play an important role in the evolution and spread of herbicide resistance [8].

Mechanisms of herbicide resistance in weeds can be broadly classified into two categories [8, 9] (i) modifications in the herbicide target enzyme (target-site resistance; TSR) and (ii) mechanisms not involving the target enzyme (non-target-site resistance; NTSR). TSR is typically conferred by single major-effect alleles, whereas NTSR is believed to be conferred by multiple small-effect alleles [9]. The TSR mechanisms largely involve mutation(s) in the target site of action of herbicide, resulting in an insensitive or less-sensitive target protein of the herbicide. In such cases, TSR is primarily determined by monogenic traits. Additionally, TSR can also evolve as a result of the over-expression or amplification of the target gene. TSR mechanisms alter the amino acid sequence and/or expression level of the target enzyme, reducing the herbicide’s ability to inhibit the enzyme or requiring a greater herbicide concentration to achieve adequate inhibition [10]. TSR to acetolactate synthase (ALS) inhibitors and acetyl-CoA carboxylase (ACCase) inhibitors, two large classes of herbicides used to control grass weeds, is the most widely documented mechanism of resistance [4]. On the other hand, NTSR mechanisms include all mechanisms that reduce the concentration of active herbicide remaining available to interact with the target site protein, as well as mechanisms that allow the plant to cope with inhibition of the target site [10]. NTSR mechanisms include reduced herbicide uptake/translocation, increased herbicide metabolism, decreased rate of herbicide activation, and/or sequestration [10, 11] (Figure 1).

Figure 1.

Weeds can evolve resistance to a herbicide by reducing its absorption, altering translocation and/or sequestration, or developing rapid necrosis of the foliage via degradation of the active ingredient. Source: [12].

3.1 Non-target site resistance (NTSR) mechanisms in weed species

Mechanisms that can contribute to NTSR are complex and involve several different gene types and families. This molecular and genetic complexity makes the identification of particular genes involved in NTSR difficult. Recent advances in this area have identified putative NTSR genes contributing to enhanced herbicide metabolism [13].

3.1.1 Metabolism-based NTSR

Plants contain large numbers of genes encoding enzymes that perform biochemical reactions for the synthesis of secondary metabolites and for detoxifying xenobiotic compounds (e.g., herbicides) [14]. Herbicide metabolism is the degradation of herbicide molecules by endogenous plant enzymes. Metabolism-based NTSR involves increased the activities of enzyme complexes including esterases, cytochrome P450s (CYP450s), glutathione S-transferases (GSTs), and/or Uridine 5′-diphospho (UDP)-glucosyl transferasesm [8]. NTSR, if it involves herbicide detoxification by these enzymes, is usually governed by multiple genes (polygenic) and may confer resistance to herbicides with completely different modes of action [15]. Enhanced rates of herbicide metabolism in NTSR are, in general, have a three-phase process [12, 16].

Phase I reactions increase the polarity of the herbicide and involve oxidation, reduction, or hydrolysis, which form free amino, hydroxyl, or carboxylic acid groups The most common phase I reactions are oxidation reactions carried out by cytochrome P450 monooxygenases (P450s). P450s are a large superfamily of enzymes and catalyze oxygen- and NADPH-dependent monooxygenase reactions [8, 12, 16].

Phase II reactions are commonly catalyzed by the glutathione S-transferase (GST) superfamily that is large and diverse. Higher plants have at least 10 different GST classes, of which the predominant phi and tau classes have broad substrate specificities and are primarily responsible for herbicide detoxification. GSTs conjugate glutathione to oxidized xenobiotics and individual GSTs of several classes are key players in NTSR to herbicides. The best-characterized role of GSTs in NTSR is for the “Peldon” MHR Alopecurus myosuroides populations that are resistant to the photosystem II inhibitor chlorotoluron and several ACCase-inhibiting herbicides. The glycosyltransferase enzyme family is also involved in phase II of herbicide metabolism. Specifically, glycosyltransferases conjugate herbicides directly or conjugate a sugar molecule to a variety of lipophilic molecules including xenobiotics. Glycosyl transferases have been shown to metabolize many herbicides and have important roles in conferring tolerance to other abiotic stresses such as salt, cold, and drought, by modifying anthocyanin accumulation [12, 16].

The third phase of herbicide metabolism involves compartmentalization and transportation of the conjugated herbicide into the vacuole or extracellular space [17]. The most common transporters in phase III are ABC transporters. ABC transporters have been shown to transport herbicide metabolites of primisulfuron, glutathione-conjugated herbicide metachlor, and have potential roles in conferring NTSR to glyphosate in Conyza canadensis (Figure 2).

Figure 2.

Herbicide metabolized in three phases. (a) Initially, herbicide is subjected to a redox reaction to increase its hydrophilicity (phase I). This metabolized herbicide is further processed into phase II. Metabolism may be concluded with the storage of metabolized compounds (phase III). Sources: [15].

3.1.1.1 Acetyl CoA carboxylase (ACCase)-inhibitors

Acetyl CoA carboxylase is a very crucial enzyme, which involves in the formation of malonyl CoA via the carboxylation of acetyl CoA [8]. Malonyl CoA is needed for de novo fatty acid biosynthesis, which is essential for plant survival. ACCase-inhibitors impair malonyl CoA formation in some grass species and ultimately lead to plant death [8]. Research results found metabolic resistance to ACCase-inhibiting herbicides has occurred on many weed plants including Asia minor bluegrass, barnyard grass, blackgrass, Italian ryegrass, Japanese foxtail, rigid ryegrass, and wild oat. In the majority of these cases, enhanced metabolism mediated by CYP450s was reported. For instance, rapid degradation of diclofop-methyl was observed in rigid ryegrass populations from Australia. Interestingly, exposure to low doses of diclofop-methyl acid application is rapidly selected for metabolic resistance in rigid ryegrass. Moreover, the metabolites produced in these resistant plants were found to be similar to those in wheat formed via ring hydroxylation and sugar conjugation. This result suggests that in resistant grasses, the metabolism of ACCase-inhibitors occurs through a wheat-like detoxification pathway mediated by CYP450s [8].

3.1.1.2 Acetolactate synthase (ALS)-inhibitors

Enhanced metabolism conferring resistance to ALS inhibitors has been documented in some grass and broadleaf weeds, such as barnyard grass, common waterhemp, Palmer amaranth, rice barnyard grass, rigid brome, short awn foxtail, and water chickweed [8]. Numerous studies have also elucidated the molecular basis of metabolic resistance to ALS inhibitors. Most of the studies have predominantly identified multiple CYP450 genes that are either constitutively expressed or upregulated. For example, the mechanism of mesosulfuron-methyl resistance in short-awn foxtail was studied and two CYP450 genes (CYP94A1 and CYP71A4) were overexpressed in the resistant plants. In a similar, two CYP450 genes, (CYP81A12 and CYP81A21) were identified as candidate genes conferring resistance to bensulfuron-methyl and penoxsulam in rice barnyard grass. Several CYP450 genes mediating NTSR to ALS inhibitors have been identified in water chickweed, ryegrass, flaxseed, and blackgrass. In addition to CYP450s, involvement of GSTs, GTs, and ATP-binding cassette (ABC) transporters has also been reported. For instance, in ALS-inhibitor-resistant water chickweed, four genes including three CYP450s and an ABC transporter were highly expressed in all resistant plants [8].

Recently, a new resistance mechanism in weeds has been identified. Glyphosate resistance is possible through aldo-ketoreductase (AKR)-based metabolism [18], upregulation of an ABC membrane transporter pumping out glyphosate outside the cell [19], and programmed cell death causing rapid necrosis [20]. Similarly, 2,4-D resistance due to either CYP-450-based metabolism [21], a double point mutation [22] or 9-codon deletion in an auxin transcriptional repressor [23], or rapid necrosis [24] has also been reported. These recent findings depicted that herbicide selection for many survival mechanisms will occur and increase the chances for plants to harbor multiple resistance mechanisms.

3.1.1.3 Photosystem II (PSII) inhibitors

The PSII complex is located within the thylakoid membranes of chloroplasts and contains two proteins, D2 and D1 [25]. PS-II inhibitors act by competitively binding to the plastoquinone binding site (QB) on the D1 protein in the PS-II complex of the chloroplast. Once a PSII-inhibiting herbicide binds, it blocks the transfer of electrons from plastoquinone QA in D2 to plastoquinone QB in D1, which prevents CO2 fixation and production of ATP and NADPH. Blocking electron transport leads to the production of reactive oxygen species (ROS), which destroys cell integrity [15, 25]. Some herbicide chemical groups such as triazines, triazinones, and ureas inhibit Photosystem II [15]. Till now, 74 weed species have been reported to develop resistance to PS-II inhibitors across the globe, through both TSR and NTSR mechanisms [25]. NTSR to PS-II inhibitors have been reported in many weed species including bluegrass, common ragweed, common water hemp, Palmer amaranth, and wild radish. The metabolism of PS-II inhibitors was catalyzed by increased activity of GST enzymes and/or CYP450 enzymes [25].

3.1.2 Reduced herbicide absorption

To be effective, herbicides must be absorbed into cells of plants through the roots, in the case of soil-applied herbicides, or from the leaves in the case of foliar-applied herbicides. During herbicide application, herbicide droplets must land on the leaf surfaces and overcome a number of barriers before cellular uptake. This passive process largely depends on leaf surface characteristics, herbicide chemical properties, and their interactions. Herbicide absorption from cellular uptake, where absorption is the process of overcoming the physical barrier of leaves (i.e., cuticle) before the herbicide reaches the apoplast, and uptake is the movement of herbicide from the apoplast into plant cells. Herbicide-resistant weed populations exhibit reduced herbicide absorption, characterized by a reduction in the penetration via the cuticle before reaching the epidermis, whereas cell walls do not pose a significant resistance to cellular uptake. Reduced absorption is not a common NTSR mechanism; however, it has occurred in both dicots and monocots to some herbicide groups such as synthetic auxins and 5-enolpyruvylshikimate-3-phosphate synthase inhibitors [15].

Differences in root absorption of herbicides between species have been associated to root morphology differences. There are no cases of evolved resistance to soil-applied herbicides due to reduced root absorption [26]. Differences in foliar absorption of herbicides between weed plants have been highly associated with leaf anatomical structure than biochemical differences [10]. Differential foliar absorption of herbicides between species was directly linked to differences in cuticle thickness and/or composition; however, the number and/or structures of leaf features such as trichomes and hairs have also been involved. For instance, Hirsute leaves are covered with hairy trichomes that can retain spray droplets better than smooth, hairless, or glandless cuticles, hence facilitating absorption. Other leaves have lysigenous glands involved in the production and storage of oily secondary metabolites that can compartmentalize lipophilic herbicides, preventing them from reaching their site of action [26].

Decreased absorption is uncommon NTSR mechanism; however, it has been reported with the resistance of common sunflower to imazethapyr and chlorimuron, prickly lettuce to 2,4-D, annual bluegrass to atrazine, and L. multiflorum to glyphosate. No differences were found in cuticular wax amount per unit area of leaf surface between two biotypes of L. multiflorum with a threefold difference in glyphosate susceptibility and reduced absorption in the less sensitive biotype. When reduced absorption is implicated, it is most often only one contributing factor to the overall resistance mechanism. For example, resistance to glyphosate in A. tuberculatus biotypes was due to both reduced absorption and a herbicide resistance allele of the glyphosate enzyme target EPSPS [12].

3.1.3 Reduced translocation and sequestration

Many foliar-applied systemic herbicides rely on translocation through the phloem. These herbicides must overcome the cuticle barrier and enter the cells of mature source leaves (symplast). This transport can involve active and/or passive diffusion processes [12]. Once inside the symplast, systemic herbicides translocate from source leaves to younger sink leaves via the phloem [16]. Herbicide resistance due to reduced translocation occurs when the herbicide is contained in source leaves and prevented from translocating to young leaves. Mechanisms that trap the herbicide in source leaves (e.g., through sequestration within vacuoles of leaf trichomes) or prevent its normal movement to the growing points across membrane barriers (through altered activity of active membrane transporters) will reduce the total amount of herbicide translocated, thus conferring resistance [12]. Therefore, alterations of translocation patterns can lower herbicide efficacy. Herbicide resistance as a result of reduced translocation has been observed in grass weed species, such as Lolium spp. [15]. Reduced translocation of glyphosate is the most common type of NTSR mechanism [27]. In these plants, the amount of glyphosate delivered to the meristems is lower than what is essential to be toxic to the weed plant. Reduced glyphosate translocation was first recorded in glyphosate-resistant Lolium rigidum, less glyphosate translocated to the meristems, relative to glyphosate-susceptible L. rigidum [28]. Glyphosate-resistant C. canadensis had reduced translocation [27]. This is due to differences in the cellular distribution of glyphosate and subsequent phloem loading and translocation. In these biotypes, glyphosate enters the source leaves normally; however, it cannot translocate to the meristems because it is rapidly sequestered within the vacuole [29]. Vacuole sequestration activity is temperature-dependent, with less sequestration observed in C. canadensis under lower temperatures (Figure 3) [30].

Figure 3.

Reduced herbicide translocation due to vacuolar sequestration. Source: [15].

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4. Conclusion

Managing weeds in crop production, whether infield, greenhouses, or containers, can be challenging and costly practice; however, it is essential to successful production. Weeds not only compete with the crop for plant nutrients and sunlight but also host plant pathogens. Herbicides are used in many crop production areas as an economical option to control weeds. By using herbicides before weeds emerge, weed competition with the crop can be reduced or eliminated, resulting in higher quality yield and less labor costs. However, their extensive utilization across the globe imposes strong selection pressure, which results in resistant weed population development. Herbicide resistance is a rapidly growing worldwide problem that causes significant crop yield loss and increases production costs. The most common herbicide resistance form is target-site resistance and non-target site resistance. Non-target site herbicide resistance is complex and involves several different gene types and families. This molecular and genetic complexity makes the identification of particular genes involved in NTSR difficult. Non-target site resistance mechanisms include reduced herbicide uptake/translocation, increased herbicide metabolism, decreased rate of herbicide activation, and/or sequestration. Lack of new herbicides in the market makes utilization of already available herbicides inevitable. Therefore, it is very imperative to integrate various weed management practices to curve a rapid increase in non-target site resistance development. It is equally important to reduce application of the same kind of herbicide over time to overcome resistance to weed population establishment.

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Written By

Ermias Misganaw Amare

Submitted: 20 April 2022 Reviewed: 05 May 2022 Published: 01 February 2023