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Introduction to Herbicide Metabolism, Resistance, and Related Concepts

Vijay K. Nandula

USDA-NIFA, Kansas City, Missouri, USA

1.1 Introduction

Weeds were in existence even before humans took up the cultivation of plants for food, feed, fuel, and fiber. Before the advent of synthetic organic-based herbicides in the 1940s, weeds were controlled for thousands of years by mechanical, cultural, and biological means. 2,4-Dichlorophenoxyacetic acid (2,4-D) was the first herbicide to be used selectively to control weeds. Since then, several herbicides belonging to different chemical classes and possessing diverse modes of action have been synthesized and commercialized around the world. Herbicides have widely contributed to increasing world food production in an efficient, economical, and environmentally sustainable manner. However, repeated application(s) of the same herbicide or a different herbicide with a similar mode of action on the same field, growing season after growing season, has contributed to the widespread occurrence of resistance to herbicides in several weed species. Currently, there are 534 unique cases (species × site of action) of herbicide-resistant weeds globally, with 273 species (156 dicots and 117 monocots); weeds have evolved resistance to 21 of the 31 known herbicide sites of action and to 168 different herbicides; and herbicide-resistant weeds have been reported in 102 crops in 75 countries.1

One of the most important phases after the confirmation of herbicide resistance in a weed population is the deciphering of the underlying resistance mechanism(s). The mechanism of resistance to herbicide(s) in a weed population can greatly determine the effectiveness of resistance management strategies. For example, a target site mutation could endow cross-resistance to herbicides with similar mechanism of action, or metabolic resistance can bestow the ability to survive herbicides across more than one mechanism of action. In general, mechanisms of resistance to herbicides are broadly categorized into target-site- and non-target-site-based mechanisms. The major category in the non-target-site-based mechanisms is resistance via the metabolism/breakdown of herbicide molecules to non-phytotoxic metabolites that are further subject to conversion to secondary compounds that are also found in plants.

1.2 Herbicide Resistance and Tolerance

The Weed Science Society of America (WSSA)2 defines herbicide resistance and herbicide tolerance as follows. Herbicide resistance is the inherited ability of a plant to survive and reproduce following exposure to a dose of herbicide normally lethal to the wild type. In a plant, resistance may be naturally occurring or induced by techniques such as genetic engineering or the selection of variants produced by tissue culture or mutagenesis. Herbicide tolerance is the inherent ability of a species to survive and reproduce after herbicide treatment. This implies that there is no selection or genetic manipulation to make the plant tolerant as it is naturally tolerant.

The natural tolerance of many crops to herbicides is thus exploited through the concept of herbicide selectivity, which is the ability of an herbicide to kill or slow the growth of some plants (weeds) without affecting others (crops). Herbicide selectivity or tolerance is mostly determined by the ability of a crop plant to metabolize an herbicide to non-phytotoxic metabolites. Metabolism of herbicides usually occurs in three phases: a conversion of the herbicide molecule into a more hydrophilic metabolite (phase 1), followed by conjugation to biomolecules such as glutathione/sugar (phase 2), and further conjugation/breakup/oxidation reactions followed by transport to vacuoles or cell walls where additional breakdown occurs (phase 3).3-5

Safeners. In general, safeners are chemicals applied in combination with herbicides to provide tolerance to grass crops such as wheat, rice, corn, and sorghum against certain thiocarbamate, chloroacetamide, sulfonylurea, and aryloxyphenoxypropionate herbicides that are applied preemergence or postemergence. Safeners enhance herbicide detoxification in "safened" plants. Safening agents activate/catalyze cofactors such as glutathione and enzyme systems such as cytochrome P450 (CYP) monooxygenases, glutathione-S-transferases (GSTs), and glycosyl transferases.6 The safener-mediated induction of herbicide-detoxifying enzymes appears to be part of a general stress response.4, 6 These enzymes deactivate herbicide molecules by modifying side chains, which are then conjugated to biochemical moieties such as sugar and amino acid residues. Some of these conjugates are further deposited in vacuoles and cell walls.

1.3 Layout of Content in the Following Chapters

1.3.1 Chapter 2: Synthetic Auxin Herbicide-Tolerant Crops

This chapter reviews the overarching processes and approaches utilized for the discovery of 2,4-D- and dicamba-tolerant trait technologies. Additionally, this chapter discusses deregulation, adoption, potential future challenges, and opportunities with these two synthetic auxin herbicide-tolerant trait technologies.

1.3.2 Chapter 3: Metabolic Degradation of Glyphosate in Soil Microbes, Endophytes, Crops, and Weeds

Glyphosate is the most used herbicide worldwide. Both microbes and plants can metabolize it by various enzymes. This chapter comprehensively reviews the metabolic fate of glyphosate in soil microorganisms, endophytes, crops, and weeds.

1.3.3 Chapter 4: Enhanced Metabolic Resistance to Herbicides in Alopecurus myosuroides (Black Grass)

Black grass is a major problem weed of winter cereals in Northern Europe, which is difficult to control with herbicides due to the rapid evolution of non-target-site resistance (NTSR) to selective herbicides. Enhanced metabolic resistance (EMR) underpins NTSR in black grass and is correlated with the increased expression of CYPs, GSTs, UDP-glucose-dependent glycosyltransferases (UGTs), and ATP-binding cassette (ABC) transporters that act concertedly to detoxify herbicides. In this chapter, the role of these proteins in herbicide metabolism and EMR in black grass is reviewed, along with an analysis of their respective gene diversity and an assessment of likely members involved in NTSR.

1.3.4 Chapter 5: Herbicide Detoxification in Black Grass

This chapter provides additional insights into the metabolic mechanisms of resistance in black-grass populations in Europe.

1.3.5 Chapter 6: Metabolism-Based Resistance in Lolium rigidum and Raphanus raphanistrum

L. rigidum Gaud. (annual ryegrass) and R. raphanistrum L. (wild radish) are abundant, widespread, and economically damaging weed species across the grain-cropping regions of southern Australia. Multiple herbicide resistance because of sequential selection and/or gene flow is prevalent in populations of these two outcrossing weed species, conferred by both target-site and non-target-site resistance mechanisms. This chapter focuses on recent studies involving these two species that investigated herbicide resistance conferred by enhanced metabolism, which can simultaneously compromise the efficacy of herbicides from different sites of action.

1.3.6 Chapter 7: Management of Metabolism-Based Resistance in Lolium rigidum in Australia

This chapter reviews the development and adoption of novel herbicide resistance management strategies to combat resistant L. rigidum populations across cropping regions of Australia.

1.3.7 Chapter 8: Metabolic Herbicide Resistance in Echinochloa phyllopogon

This chapter reviews almost 20?years of collective research efforts on a multiple herbicide-resistant (MHR) line of E. phyllopogon (syn. Echinochloa oryzicola), a noxious grass weed in rice fields, which has developed resistance to at least 15 herbicides from 10 chemical classes due to metabolism-based mechanisms.

1.3.8 Chapter 9: Metabolic Resistance to Herbicides in Echinochloa crus-galli (and Echinochloa colona)

This chapter reviews past and recent research on multiple herbicide-resistant Echinochloa colona and Echinochloa crus-galli populations in the United States and around the world with a focus on metabolic resistance mechanisms.

1.3.9 Chapter 10: Metabolic Resistance to HPPD-Inhibiting Herbicides in Dioecious Amaranthus Species

This chapter discusses the current state of knowledge regarding the occurrences of and metabolic basis for resistance to various 4-hydroxyphenylpyruvate dioxygenase (HPPD)-inhibiting herbicides in dioecious Amaranthus spp., including descriptions of molecular genetic, biochemical, and physiological aspects of resistance.

1.3.10 Chapter 11: Overview of Metabolism-Based Resistance to PS-II Inhibitors in Weed Species

Photosystem (PS) II...