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1995 Herbicide-Resistant Field Crops Jack H. Dekker Iowa State University, [email protected]

Stephen O. Duke United States Department of Agriculture

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Abstract This chapter reviews information about how crop plants resist herbicides and how resistance is selected for in plants and surveys specific herbicide-resistant crops by chemical family. The discussion in the chapter includes HRCs derived from both traditional and biotechnological selection methodologies. Plants avoid the effects of herbicides they encounter by several different mechanisms. These mechanisms can be grouped into two categories: those that exclude the herbicide molecule from the site in the plant where they induce the toxic response and those that render the specific site of herbicide action resistant to the chemical. The chapter presents herbicide-resistant crops by the herbicide chemical family—such as, triazine, acetolactate synthatase, acetyl-CoA carboxylase, glyphosate, bromoxynil, phenoxycarboxylic acids, and glufosinate. Resistant crops are listed in the chapter regardless of whether they have been commercialized or were developed for experimental purposes only, and are provided regardless of their “success” as resistant plants.

Disciplines Agricultural Science | Agriculture | Agronomy and Crop Sciences | Weed Science

Comments This article is from Advances in Agronomy 54 (1995): 69–116, doi:10.1016/S0065-2113(08)60898-6.

Rights Works produced by employees of the U.S. Government as part of their official duties are not copyrighted within the U.S. The onc tent of this document is not copyrighted.

This article is available at Iowa State University Digital Repository: http://lib.dr.iastate.edu/agron_pubs/11 HERBICIDE-RESISTANTFIELD CROPS

Jack Dekker ' and Stephen 0. Duke?

I Agronomy Department Iowa State University Ames, Iowa 5001 1 'United States Department of Agriculture Agricultural Research Service Southern Weed Science Laboratory Stoneville, Mississippi 38776

I. Introduction 11. Mechanisms of Herbicide Resistance A. Exclusionary Resistance Mechanisms B. Altered Molecular/C~ellularSite (Target) of Herbicide Action C. Site of Action Overproduction 111. Selection for Herbicide-Resistant Variants A. Sources of Resistance Genes and Traits B. Traditional Plant-Breeding Techniques C. Biotechnological Techniques W. Herbicide-Resistant Crops by the Herbicide Chemical Family A. Triazines B. Acetolactate Synthatase Inhibitors C. Acetyl-CoA Carboxylase Inhibitors D. Glyphosate E. Bromoxynil F. Phenoxycarboxylic Acids (e.g., 2,4-D) G. Glufosinate (Phosphinothricin) H. Other Herbicides V. Summary References

I. INTRODUCTION

Traditionally, herbicidal chemicals have been selected for their weed-killing characteristics as well as for their effects on crops. One of the primary limitations in this search has been lack of tolerance to the chemical by one or more of the major world crops (e.g., rice, maize, soybean, wheat, rapeseed). Also, this process

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Advonces in Agmnom.v Vor'ume 14 Copyright 0 1995 by Acadernlc Press. Inc. All rights of reproduction in any form reserved. 70 J. DEKKER AND S. 0. DUKE has led to the development of herbicides that often control only part of the weed species present in that crop, necessitating the use of other herbicides or management strategies. Herbicides that control a broad spectrum of weed species often have limited utility because they also injure crops. Additionally, often the most desirable herbicides for weed control and crop safety have other less desirable characteristics (e.g., environmental, economic). For these and other (e.g., regulatory) reasons, herbicide development has been very expensive, time consuming, and has yielded a relatively small number of chemicals with desirable agronomic, environmental, and economic qualities from a potentially large group of candidates. With the availability of many new biotechnological tools to incorporate herbicide resistance into crops, this traditional approach has been reversed in some instances. The possibility now exists to select herbicides for desirable weed control, as well as environmental and economic qualities at the beginning of the discovery process, and incorporate resistance into the crop(s) after these herbicides have been identified. The development of herbicide-resistant crops (HRC) could provide many advantages in the efficient, safe, and economical production of crops, although there may be risks involved in the development of specific technologies (Bright, 1992; Dekker and Comstock, 1992; Duke et al., 1991; Dyer et al., 1993b; Goldburg et al., 1990; Goodman, 1987; Hindmarsh, 1991; Kline, 1991; Miller, 1991; William- son, 1991). Assessment of the risks and benefits of individual HRCs is complex, and value judgements about the appropriate utilization of HRCs have been pur- posefully avoided in this chapter. Several environmental advantages may result from the development of HRCs. Herbicides and their associated HRCs could be developed with less persistence in the environment (e.g., herbicide “carryover” to subsequent crops in a rotation; accumulation in other sites in the landscape, bio- sphere), less damage to off-site targets (e.g., adjacent susceptible crops; homes and farmsteads; surface waters), decreased undesirable movement in the environment (leaching downward through the soil profile to subsoil, groundwater sites; volatility and movement to off-target sites), and low acute and chronic toxicity to humans and animals. Also, these technologies could result in several advantages to crop producers, including less expensive production costs. HRC systems could result in increased production options to growers by providing more weed control strategies, resulting in an increased likelihood of the use of multiple, inte- grated approaches to weed management. For these and other reasons, crop germ plasm improvement now also includes selection and incorporation of desirable herbicide-resistance qualities. Conversely, production and utilization of crops resistant to herbicides with undesirable characteristics could have adverse toxicological and environmental consequences. However, there is comparatively little effort being expended to generate and develop crops resistant to herbicides that might raise such concerns. HERBICIDE-RESISTANTFIELD CROPS 71

The term herbicide resistance is used to describe the ability, trait, or quality of a population of plants within a species or larger taxon, or of plant cells in culture, to withstand a particular herbicide at a dosage that is substantially greater than the wild type of that plant is able to withstand, with a near normal life cycle. Herbicide resistance can be conferred in many ways and includes the pre-existing lack of susceptibility, selection of resistant variants from within a diverse species, or resistance achieved by genetic manipulation (e.g., crops). Because of the diversity of possible mechanisms, a complete description requires the use of appropriate qualifiers to the term “resistance.” This chapter reviews information about how crop plants resist herbicides and how resistance is selected for in plants and surveys specific herbicide-resistant crops by chemical family. The scope of this discussion includes HRCs derived from both traditional and biotechnological selection methodologies. The toxicological and environmental concerns that have been raised and discussed in other reviews (e.g., Dekker and Comstock, 1992; Duke et al., 1991; Dyer et al., 1993a,b) will not be discussed here. The following discussion reviews a very large literature, but emphasizes that information relevant to field crop improvement.

II. MECHANISMS OF HERBICIDE RESISTANCE

Plants avoid the effects of herbicides they encounter by several different mechanisms (Holt et al., 1993; Vaughn and Duke, 1991). These mechanisms can be grouped into two categories: those that exclude the herbicide molecule from the site in the plant where they induce the toxic response (exclusionary resistance) and those that render the specific site of herbicide action resistant to the chemical (site of action resistance). Several of these mechanisms often act in concert to produce whole-plant resistance. Although it is difficult to generalize over the many plant species affected by the use of herbicides in crop production (weeds and crops), differential resistance is primarily due to herbicide metabolism, sec- ondarily due to site of action mechanisms, and lastly due to differences in inter- ception and absorption (Devine ef al., 1993a.b). In general, our understandings of plant physiology, morphogenesis, and biochemistry are significantly less than our understanding of herbicides. This situation limits the options available for crop improvement by enhancement of herbicide resistance. Herbicides with a single site of action in plants have been the focus of the first HRCs being developed because they rely on single gene mutants, or single gene transformants, for resistance. As our understanding of plant biology increases, more targets for crop improvement, especially quantitative traits, will become available. 72 J. DEKKER AND S. 0. DUKE

A. EXCLUSIONARYRESISTANCE MECHANISMS

The specific site at which herbicides act is protected to some extent by the morphology and physiology of the individual plant species and subspecific vari- ant. The structural characteristics of the leaf, root, and vascular system influence the movement of herbicides into and through the plant. The metabolic activities in living plant cells also are capable of detoxifying herbicides. At the present time, the only exclusionary strategy for HRC production is to transform plants with genes encoding enzymes that degrade herbicides.

1. Herbicide Uptake

Herbicides typically are encountered by the plant at the soil-root, or leaf-air, interfaces. Differential absorption, adsorption, and uptake of the herbicide into the plant at these interfaces can occur (Hess, 1985). Herbicides must pass the nonliving portions (apoplast) of the plant and enter the living parts (symplast) of the plant to have an effect. Herbicide resistance can be conferred in individual plant species by structures capable of excluding the entry of these chemicals into the living part of the plant. The first plant structures that encounter herbicides are nonliving and include those associated with the leaf, stem, and root surfaces. Movement of a herbicide across these nonliving structures is complex and involves the nature of the herbicide applied (including the formulation ingredients), the physical properties of the cuticle (epicuticular wax, cuticular wax, cutin, pectin fibers, cell walls, and the cuticular “peg” between cell walls), the species and age of the plant, and the environment (Devine et al., 1993a,b). Herbicide absorption by the plant from the soil solution can occur through root, shoot, or seed tissue. Root absorption occurs through passive diffusion of the soil solution through the epidermis (suberized in older root tissue) and cortex. These outer structures are separated from the root endodermis (containing the vascular tissues in the stele) by a suberized layer, the Casparian strip. Herbicide uptake can occur anywhere in the root system, but absorption primarily occurs at the apical end (Jacobson and Shimabukuro, 1982; Strang and Rogers, 197 1). It is in this area of the root system that most water and ion uptake takes place, the place where the Casparian strip is least developed (Tanton and Crowdy, 1972). Despite the important role herbicide uptake through shoots and roots plays in the total resistance of a plant to a herbicide, it is not generally regarded as a primary crop improvement target for enhancing herbicide resistance. It more likely plays a secondary role in conjunction with other plant factors, the sum of which act to produce the whole-plant level of herbicide resistance. Once the complex chemical nature of leaf waxes (i.e., epicuticular, cuticular) is better understood, and once the exact nature of herbicide HERBICIDE-RESISTANTFIELD CROPS 73 uptake by roots in specific crop species is well characterized, it is conceivable that structures modified by single (or few) genes could be the focus of selection schemes.

2. Translocation

After herbicides are taken into the plant they often are transported to the site of activity. This movement can be either in nonliving (apoplast; eg., cell walls, xylem) or in living tissues (symplast; e.g., cell plasmalemma, phloem). This translocation of herbicides can either be over relatively short distances (e.g., paraquat activity in living cells near the point of entry) or it can be accomplished by the vascular system over relatively longer distances (e.g., glyphosate translocation in the phloem). Whether a particular herbicide is moved over short or long distances, and what plant structures facilitate or retard its movement, is a function of the chemical nature of the herbicide, the plant species, the condition of the plant (e.g., age, stress, nutrition, etc.), and the environment in which both are found. Al- though much of the physiological and morphological effects of the plant on herbicides are understood (Devine et al., 1993a), it has been far easier to modify the chemical properties of the herbicide (Crisp and Look, 1978; Crisp and Larson, 1983; Lichtner, 1986) for resistance than it has been to alter the translocation factors in the plant. Additionally, differential translocation of herbicides within different plant species is intimately related to concurrent herbicide metabolism, a confounding factor when studying translocation resistance mechanisms. For these reasons, crop improvement by alteration of solute translocation factors in crop plants will probably remain a low priority for the enhancement of herbicide resistance. In few cases of herbicide resistance has translocation proven to be a significant factor.

3. Compartmentation

Herbicides can be sequestered in several plant locations before they reach the site of action. Some lipophilic herbicides may become immobilized by partition- ing into lipid-rich glands or oil bodies (Foy, 1964; Stegink and Vaughn, 1988). Sequestration of herbicides in vacuoles, followed by metabolism, is another possible mechanism of resistance by immobilization (Coupland, 199 1). Differential metabolism of herbicides has been reported in cell vacuoles from soybean suspension cultures of both susceptible and resistant variants (Schmitt and Sandermann, 1982). Sequestration (Fuerst et al., 1985; Norman et al., 1993), metabolism (Am- sellem eral., 1993; Shaaltiel eral., 1988), or both (Lehoczki eral., 1992) has been suggested as the possible basis of paraquat resistance in weedy Conyza spp. As with uptake and translocation, herbicide resistance enhancement by manipulation 74 J. DEKKER AND S. 0. DUKE of these complex, poorly understood, physiological phenomena will probably remain an insignificant objective for crop improvement for some time.

4. Metabolic Detoxification

One of the most useful mechanisms of resistance for crop improvement is the enhancement of herbicide metabolism to detoxify the chemical before it reaches the site of inhibition. Metabolic detoxification of herbicides and other chemicals by plants are the major mechanisms providing resistance in crops, and this topic been extensively reviewed (e.g., Baldwin, 1977; Casida and Lykken, 1969; Cole et al., 1987; Devine et al., 1993a; Fedtke, 1982; Hatzios and Penner, 1982; Kear- ney and Kaufman, 1975; Lamoureux and Frear, 1979; Menzer, 1973; Owen, 1987; Sanderman et al., 1977; Shimabukuro et al., 1982; Shimabukuro, 1985). Crop enhancement by herbicide detoxification can be accomplished either by selection for variants or mutants with increased levels of specific metabolic activities or by introduction and transformation of crop plants with genes from other organisms. Herbicide safeners, antidotes, antagonists, protectants, or synergists are herbi- cidally inactive chemicals that are applied to crops and weeds for improved weed control. Many types of these chemicals exist, but often they are used to enhance the action of a herbicide by either interfering with weed metabolism (hence improved weed control) or enhancing crop metabolism (hence crop protection) (Ezra et al., 1985; Lamoureux and Rusness, 1986). The reader can refer to some related reviews (Devine et al., 1993a; Pallos and Casida, 1978) for a discussion of this approach to crop improvement. The biochemical reactions that detoxify herbicides can be grouped into four major categories: oxidation, reduction, hydrolysis, and conjugation. Oxidation of herbicides is among the most important detoxification reactions providing resistance in plants. These reactions are catalyzed by monooxygenases known as mixed function oxidases and include alkyl oxidation, aromatic hydroxylation, epoxidation, N-dealkylation, 0-dealkylation, and sulfur oxidation. Much of the biochemistry of these reactions has not been characterized, but aryl hydroxylation may be the most common reaction leading to herbicide detoxification (Shimabukuro, 1985). Reduction of herbicides is of much lesser importance in plants compared to other metabolic reactions conferring resistance. Aryl nitroreduction is an important reaction in herbicide degradation, but probably plays a minor role in herbicide detoxification, and may compete with the more important glutathione conjugation reaction (Lamoureux and Rusness, 198 I). Hydrolysis of herbicides is a common plant reaction and is important in detoxification of several herbicides, including bromoxynil (Buckland et al., 1973), cyanazine (Benyon et al., 1972), and propanil (Lamoureux and Frear, 1979), as €IERBICIDE-RESISTANT FIELD CROPS 75

well as other ester, amide, and nitrile-containing herbicides. Carboxylic acid ester herbicides such as 2,4-D (ester; Loos, 1975), as well as several graminicides such as diclofop-methyl (Fedtke and Schmitt, 1977; Shimabukuro et al., 1979), are hydrolyzed to the active, free acid once in the plant leaf (Loos, 1975). Conjugation of herbicides to glucose, amino acids, or glutathione is a major reaction in detoxification and is a potentially major objective for crop resistance improvement. Conjugation in plants is the reaction in which a herbicide metabo- lite formed in earlier reactions is joined with an endogenous substrate to form a new, larger compound. Typically this reaction converts a lipophilic herbicide molecule into a more water-soluble compound. This more polar compound is then subsequently metabolized, leading later to a bound herbicide residue. Glucose conjugation occurs to many herbicides (or their metabolites) with amino, carboxyl, or hydroxyl functional groups. Examples of glucose conjugation include 0-glucosides (e.g., chlorpropham; Still and Mansager, 1972), N-glucosides (e.g., propanil; Still, 1968), and glucose esters (e.g., diclofop-methyl; Shi- mabukuro et al., 1979). More complete treatment of this area can be found in Frear (1 976) and Hatzios and Penner ( 1982). Amino acid conjugation occurs primarily with acidic herbicides, through an a- amide bond (Mumma and Hamilton, 1976). For example, 2,4-D forms major glu- tamic (2,4-D-Glu) and aspartic (2,4-D-Asp) acid conjugates, as well as minor conjugates with alanine, leucine, phenylanaline, tryptophan, and valine. Glutathione conjugation often involves the reaction of the active parent herbicide molecule and glutathione (GSH), and is one of the most important types of conjugation conferring resistance in plants and has been extensively reviewed (Baldwin, 1977; Hatzios and Penner, 1982; Lamoureux and Frear, 1979; Lamou- reux and Rusness, 1981; Shimabukuro et al., 1978, 1982). This type of detoxification is important because of the wide range of potential substrates, or herbicides, that can be conjugated. This conjugation is accomplished primarily by glutathione-S-transferases with different specificities to different herbicide substrates. GSH conjugation involves a nucleophilic displacement reaction between GSH and the herbicide, resulting in direct detoxification of the active molecule. GSH conjugation reactions can also proceed nonenzymatically due to the high degree of reactivity of some herbicides (Lamoureux ef al., 1973; Leavitt and Penner, 1979). Many herbicide groups are conjugated by GSH and include a-chloroacetamides (e.g., metolachlor), diphenylethers, thiocarbamate sulfoxides, and 2-chloro-s-triazines. For example, atrazine is directly detoxified by nucleophilic displacement when a conjugation reaction occurs between it and GSH (La- moureux et d.,1973). The appearance of herbicide-resistant weeds due to enhanced GSH conjugation has been reported (e.g., velvetleaf, Abutilon theophrasti; Gronwald ef a/., 1989), as well as evidence of inter- and intraspecific variation in GSH conjugation in Setaria spp. (Wang and Dekker, 1994). 76 J. DEKKER AND S. 0. DUKE

There is relatively little interest in generating HRCs by manipulation of genes encoding plant enzymes that detoxify herbicides. The reason for this is unclear. However, the movement of microbial genes that encode herbicide-detoxifying enzymes into crops by genetic engineering is a strategy being used to produce HRCs for use with glyphosate, giufosinate, bromoxynil, dalapon, and 2,4-D. Details of the production of these HRCs can be found in the next section.

B. ALTEREDMOLECULARKELLULAR SITE(TARGET) OF HERBICIDEACTION

Resistance in plants can be due to differential sensitivity of molecular target sites, usually sites of herbicide activity and inhibition. Resistance is conferred on a plant by alteration or mutation of the different target site protein structures. Much of what is known about the molecular, biochemical, and physiological nature of these important sites of action comes from understandings gained from herbicide-resistant weeds (e.g., Holt and LeBaron, 1990; LeBaron and Gressel, 1982; Smith et al., 1988). Variability in the functional qualities of these target site mutants exists and they may be equally (e.g., sulfonylurea resistance) or less com- petitive (s-triazine resistance) than their wild types with the wild type site of action protein (e.g., Beversdorf et al., 1988). Examples of some important molecular sites of action, and the herbicides that interact with them to cause inhibition, follow. In each instance, a more complete presentation can be found in subsequent sections dealing with specific herbicide groups. The best characterized is the site of s-triazine inhibition of photosynthesis in the chloroplast. s-Triazine herbicides (e.g., atrazine, cyanazine) inhibit photosynthetic electron transport at the reducing side of photosystem 11. These herbicides bind to the reaction center D- 1 protein, the native binding site for plastoquinone (Arntzen et a/., 1987; Barber, 1987; Mattoo et al., 1989; Trebst, 1986, 1991). A key enzyme in lipid biosynthesis, acetyl-coenzyme A carboxylase (ACCase; Hanvood, 1988a) is the molecular site of inhibition of the aryloxyphenoxypropionates (e.g., diclofop-methyl) and cyclohexenedione (e.g., sethoxydim) herbicides (Burton et al., 1987; Hanvood, 1988b; Harwood et al., 1987; Secor and Czeke, 1988). These are important groups of herbicides used to control graminaceous plants. Several groups of herbicides target amino acid biosynthesis (Devine et al., 1993a; Kishore and Shah, 1988). Branched-chain amino acid synthesis (isoleucine, leucine, and valine) is inhibited by three classes of herbicides: the imidazo- hones (Shaner and O’Connor, 1991), sulfonylureas (Beyer et al., 1988; Blair and Martin, 1988; LaRossa et al., 1987), and triazolopyrimidine sulfonanilides (Ger- wick et al., 1990; Subramanian and Gerwick, 1989). All three groups have as their HERBICIDE-RESISTANT FIELD CROPS 77

molecular site of action the enzyme acetolactate synthase (ALS; also known as acetohydroxy acid synthase, AHAS).

c. SITE OF ACTIONOVERPRODUCTION

Resistance can be conferred by overproduction of the target site, diluting the herbicide that reaches the target site, thus allowing enough additional target protein to remain to complete normal functions and growth (Devine et al., 1993a; Goldsbrough et al., 1990; Rogers et al., 1983; Shah et al., 1986). Overproduction of the molecular site of action can confer resistance by either multiple copies of the gene encoding the target site protein (gene amplification; Steinrucken et al., 1986) or (and) by increased target site protein gene expression (Hollander-Czytko et al., 1988). For example, glyphosate resistance is conferred by the overproduction of 5-enolpyruvylshikimate-3-phosphatesynthase (EPSPS), a key enzyme in the pathway synthesizing many plant aromatic compounds. This strategy has been used to develop resistance, but has not been entirely successful in engineering glyphosate-resistant crops (Kishore and Shah, 1988).

111. SELECTION FOR HERBICIDE- RESISTANT VARIANTS

The selection for herbicide resistance for HRCs can be accomplished by both traditional plant breeding and biotechnological techniques. Before the advent of these newer approaches, few HRCs were developed using traditional plant breeding methodologies. HRCs derived from biotechnological techniques provide more ways for crop and cultivar improvement; these techniques have been reviewed previously (Botterman and Leemans, 1988; Fincham and Ravetz, 199 1; Goodman and Newell, 1985; Gressel, 1987, 1989, 1992, 1993; Mazur and Falco, 1989; Oxtoby and Hughes, 1989, 1990; Quinn, 1990; Schulz et al., 1990). Herbicide- resistant mutants probably occur in populations of all plant species, but the frequency of their occurrence is unknown (Warwick, 1991). Single sites of action herbicides provide the most likely candidates, often allowing for single loci mutants, or single gene transformants. Multiple sites of action resistance are the hard- est to select for and their development awaits more complete information of complex quantitative traits. Some multiple resistance plants have been observed in weedy populations (Powles and Howat, 1990). The following sections briefly review the several approaches used in the selection and incorporation of resistance in HRCs. 78 J. DEKKERAND S. 0. DUKE

A. SOURCES OF RESISTANCE GENESAND TRAITS

Microorganisms and higher plants and animals are potential sources of resistant genes. Each of these organisms presents its own set of advantages, problems, and technical considerations. The isolation of genes from microorganisms is often easier than from higher plants, but the right organism must be found first (Gressel, 1993). Crop plants are inherently resistant to many herbicides, and improvements can be made with proper selection efforts in many instances. One of the richest sources of resistance is in herbicide-resistant weeds. Many species of weeds have resistant populations, and prolonged selection enriched their frequency in many agricultural fields (Holt and LeBaron, 1990; LeBaron and Gressel, 1982; Powles and Howat, 1990). Studies of these resistant mutants have revealed many new insights about both the resistance mechanisms themselves, as well as new information about plant biological systems (e.g., atrazine: Dekker, 1993: Hirschberg et al., 1984; Trebst, 1986).

B. TRADITIONAL PLANT-BREEDINGTECHNIQUES

Historically, few HRCs have been developed with traditional plant-breeding approaches (Beversdorf, 1987; Beversdorf and Kott, 1987; Snape et al., 1987, 1990, 1991; Van Heile et al., 1970). This is probably due to the length of time needed to develop resistant cultivars relative to the patent life of a herbicide. Di- rect herbicide selection of variants within a species with enhanced resistance has been successful in many crops (Fedtke, 1991; Johnston and Faulkner, 1991). In many cases sufficient variability in herbicide response among plant populations exists from which to select improved lines (Boerboom e? aZ., 1991; Dekker and Burmester, 1988; Hartwig, 1987; Tranel and Dekker, 1992), but in other instances the amount has been insufficient (Kibite and Harker, 1991). Traditional plant- breeding methodologies (with resistance derived from weedy sources) have produced HRCs with resistance to s-triazines in rapeseed (Beversdorf and Hume, 1984) and lettuce (Mallory-Smith et al., 1993), with others coming in the future.

C. BIOTECHNOLOGICALTECHNIQUES

Selection for herbicide resistance traits, and their transfer into crops by biotechnological techniques, promises to speed development of HRCs considerably. Techniques that rely on rapid in vivo or in vitro selection and subsequent crop transformation may permit shorter times to achieve this type of crop improvement. Transformation by genetic engineering can also be rapid; however, development HERBICIDE-RESISTANTFIELD CROPS 79

of some HRCs by these methods has been slower than originally anticipated. These methodologies include cell and tissue culture selection, hybridization, microspore and seed mutagenesis, and plant transformation techniques.

1. Cell and Tissue Culture Selection

Somaclonal variation in cultured plant cells has been exploited to select herbicide resistance traits for crop improvement. Utilization of plant cell and tissue culture has provided one of the most important selection techniques for the development of HRCs (Chaleff, 1988; Chaleff and Ray, 1984; Hughes, 1983; Maliga et al., 1987). Selections for resistance using callus (maize; Anderson and Georgeson, 1989; Tubersosa and Lucchese, 1990), microspores and protoplasts (rapeseed; Swanson et al., 1988), and plant cell suspension cultures (maize; Parker et al., 1990a,b) have been used. HRCs resistant to herbicides inhibiting the ALS site of action have been developed using these techniques (Newhouse et al., 1991a,b), but in some instances resistance has been insufficient for complete crop safety (Bauman et al., 1992).

2. Hybridization

The transfer of herbicide resistance from weedy relatives to crops has been used to develop HRCs. Protoplast fusion techniques have been used to incorporate s- triazine resistance between Solanum species (Austin and Helgeson, 1987), as well as to transfer it into cytoplasmic male sterile Brassica variants (Barsby et al., 1987). s-Triazine resistance was transferred from weedy bird’s-rape (Brassica campestris; Beversdorf et al., 1980) to several Brassica crop species, including rapeseed and rutabaga (Beversdorf and Hume, 1984). Similar approaches have been used to transfer s-triazine resistance from the weedy green foxtail (Setaria viridis, subspp. viridis Briquet) to the foxtail millet crop (S. viridis, subspp. italica Briquet) (Darmency and Pernes, 1989). Sulfonylurea-resistant prickly lettuce (Lactuca serriola) has served as the source of ALS inhibitor resistance in a new cultivar of lettuce, ID-BR1 (Mallory-Smith et al., 1993).

3. Microspore (Gametophytic) and Seed Mutagenesis

One of the most powerful means of deriving novel herbicide-resistant variants for HRCs is mutagenesis. Several different approaches have been used and reviews of these techniques are available (e.g., Christianson, 1991). Mass selection of mutagenized soybean seed has been used to find herbicide-resistant crop variants (Sebastian et al., 1989). Similar approaches have been used in other crops (Dyer et al., 1993b). Microspore mutagenesis and selection have been used in rapeseed (Swanson et al., 1989). 80 J. DEKKER AND S. 0. DUKE

4. Plant Transformation

The transfer of herbicide resistance genes from various sources into crop plants has been performed using several techniques. These transgenic products rely on both target site and metabolic detoxification resistance mechanisms. A s-triazine- resistant gene construct composed of the mutant resistance coding sequence, expression level control sequences, and a transit-peptide encoding sequence resulted in a resistant transgenic tobacco plant line (Cheung et al., 1988). Glyphosate- resistant crop development has relied on a mutant E. coli gene fused to a EPSPS enzyme chloroplast transit sequence to create transgenic plants (Della-Cioppa er al., 1987). Transgenic, glyphosate-resistant cotton, rapeseed, soybean, tobacco, and tomato crops are currently in various stages of development and commercial- ization (Dyer et al., 1993b). Crops resistant to ALS-inhibiting herbicides have been developed by transfer of resistant genes between different higher plant species (Falco et al., 1989; Haughn et al., 1988; Miki et al., 1990). Metabolic detoxification resistance has been transferred from microbial species to crop plants. The bromoxynil-specific nitrilase gene, encoded by the bxn gene, has been transfered into cotton, potato, tomato, and rapeseed (Dyer el a]., 1993b). The cyanamid hydratase-encoding gene from the soil fungus Myrothecium verrucaria has conferred resistance in the transgenic tobacco product (Maier-Greiner et al., 1991). Detoxification of glufosinate by acetylation is accomplished by acetyl transferase, encoded by the bar gene from Streptomyces. This gene was fused to high expression promoters and was used to produce high levels of glufosinate resistance in transformed alfalfa, poplar, rapeseed, potato, sugar beet, tobacco, and tomato crops (De Block et al., 1987). Genes for herbicide resistance have been used as selectable markers in transformation studies (Yoder and Goldsbrough, 1994). It is not likely that such genes would be left in a crop that has not been approved as herbicide resistant.

IV. HERBICIDE-RESISTANTCROPS BY THE HERBICIDE CHEMICAL FAMILY

A. TIUAZINES

1. Introduction

The triazine herbicide family is a large and important group of herbicides that was first discovered in 1952, and first introduced commercially in 1957. The most important member of this family is atrazine, and its introduction revolutionized weed control in maize. Other triazine herbicides include ametryne, cyanazine, prometryn, and simazine. Herbicides in this group are used to control many broad- HERBICIDE-RESISTANTFIELD CROPS 81

leaf and grassy weeds, and are applied to the soil or foliage (often with oil-based adjuvants). Members of this group are used in many crops, including maize and sorghum. Atrazine is a relatively persistent herbicide in the environment, and environmental and health problems have been found with this chemical.

2. Mode of Action

The biochemical and physiological effects of atrazine in plants are similar to those caused by many of the s-triazines. Atrazine is the most commonly used s- triazine herbicide in agriculture. It is rapidly absorbed by plant roots and, to a lesser extent, by plant shoots (Esser and Marco, 1975). Once in the plant it trans- locates readily (apoplastically) in the xylem and cell walls. When translocation ceases, it diffuses into the cell cytoplasm and chloroplast. In the presence of light it preferentially attaches to a high-affinity binding site on a rapidly turned over 32- kDa protein known as the D-1 protein (Chua and Gillham, 1977). This protein is the product of the psbA gene and is a component of the photosystem I1 (PS 11) reaction center located in the thylakoid membranes (Callahan et al., 1989; Mattoo et al., 1989). Atrazine competes with quinone for separate, but overlapping, domains of this binding site (Pfister and Arntzen, 1979; Tischer and Strotmann, 1977; Velthys, 1981; Vermaas er al., 1983). In susceptible tissue, atrazine binding blocks electron transport on the reducing side of PS I1 from QA to QBwhich causes an increase in variable chlorophyll fluorescence (Trebst, 1980). The redirection of electrons away from the blocked site results in the generation of toxic oxy-radicals and other highly reactive radical species (Bolhar-Nordenkampf, 1979; Dodge, 1982). These radicals are primarily quenched by membrane lipids (autocatalytic peroxidation), and the death of localized tissue results. If enough tissue is de- stroyed, homeostasis cannot be maintained and the death of the plant follows. In many resistant species atrazine is metabolized by one of three initial reactions before it reaches the chloroplast: nonenzymatic hydroxylation, N-dealkylation, and conjugation with glutathione (Ashton and Crafts, 1981; Lamoureux et al., 1973).

3. Plant Resistance

Resistance to the s-triazine herbicides is a function of both alterations to the site of action as well as of metabolic exclusion before reaching that target site. Many of the insights and technologies that have been utilized for s-triazine resistance of both kinds come from understandings gained for studies of resistant weeds.

a. Site of Action Resistance The most important resistance mechanism in plants to the s-triazine herbicides is that conferred by alterations to the site of action, the D-1 protein in the chloro- a2 J. DEKKER AND S. 0. DUKE plast. Much of what we know of this type of s-triazine resistance comes from information gained as a result of the discovery of resistant weeds. s-Triazine resistance in weeds and higher plants was first discovered in 1969 in Senecio vul- gnris L. (Ryan, 1970). Since that time resistance has been found in 107 weed species, infesting over 3 million hectares worldwide (Dekker et al., 1991; Holt and LeBaron, 1990; Le Baron, 1991; Le Baron and Gressel, 1982). Resistance usually appeared in agricultural and industrial situations wherein s-triazine herbicides were used continuously for at least 5- 10 years and were the only weed control method used. After the discovery of s-triazine resistance, research revealed that resistance was not a function of differential herbicide uptake, translocation, accumulation, metabolism, or by differential membrane permeability (Radosevich, 1977; Radosevich and Appleby, 1973; Radosevich and DeVilliers, 1976). Genetic analyses indicated that the resistance mechanism was maternally inherited at the whole plant level (Sousa Machado et al., 1978b). This cytoplasmic inheritance was subsequently found to be at the level of the chloroplast membrane components (Darr et al., 1981). Photoaffinity labeling studies (Gardner, 1981; Pfister et al., 1981) showed that atrazine had reduced binding to the 32-kDa chloroplast protein (D-1) in the resistant biotype (Arntzen et nl., 1982; Bowes et al., 1980; Hirschberg and McIntosh, 1983; Pfister and Arntzen, 1979; Pfister et al., 1979, 1981; Steinback er al., 1981). s-Triazines do not have a high affinity for this altered site and hence electron transport in PS I1 is not blocked (Sousa Ma- chado et ul., 1978a). Resistance can result from point mutations to the psbA gene at several sites leading to amino acid substitutions in the D-1 protein product (Trebst, 1991). In addition to the direct effects, several structural and functional pleiotropic effects are associated with s-triazine resistance. Many of the structural changes in the chloroplast of these s-triazine-resistant mutants are similar to those in shade- adapted leaves (Boardman, 1977): increased thylakoid grana stacking, decreased starch content, lower chlorophyll a/b ratios, greater amounts of the chlorophyll a/b light-harvesting complex, and relatively lower amounts of the P700 chlorophyll a protein and chloroplast coupling factor (Burke et al., 1982; Vaughn, 1986; Vaughn and Duke, 1984). Chloroplast lipids differed between the resistant mutant and wild types (Blein, 1980; Burke etal., 1982; Pillai and St. John, 1981). These changes in lipid composition in the chloroplast membranes in the resistant mutants were correlated to enhanced resistance to lower temperature stress and greater fluidity at low temperatures (Pillai and St. John, 1981). The mutation to the psbA gene results in functional changes in resistant variants. These functional changes probably result as a consequence of the confor- mational changes in the quinone-binding niche and as a consequence of the secondary structural changes noted earlier. The quinone-binding pocket alterations in the mutant not only decrease atrazine-binding properties, but they also result in changes in the electron transfer properties in photosystem 11. The rate of electron HERBICIDE-RESISTANTFIELD CROPS 83 transfer in PS I1 from the acceptor QA to QHis reduced in the resistant mutant (Arntzen et al., 1979; Bowes et a/., 1980; Burke et al., 1982; Pfister and Arntzen, 1979). Several studies have demonstrated lower carbon assimilation efficiency, or lower productivity, in the resistant mutant compared to the wild type (Ahrens and Stoller, 1983; Beversdorf et a/., 1988; Conard and Radosevich, 1979; Holt, 1990; Holt et al., 1981; McClosky and Holt, 1989, 1991; Ort et al., 1983; Warwick, 199 1). Other studies have shown that the photosynthetic activity in these two may be similar (Ahrens and Stoller, 1983; Van Oorschot and van Leeuwen, 1984) or have found it greater in the resistant mutant relative than in the wild type under some environmental conditions (Dekker, 1993; Dekker and Burmester, 1992; Dekker and Sharkey, 1992).

b. Metabolic Resistance In many resistant species atrazine is metabolized by one of three initial reactions before it reaches the chloroplast: nonenzymatic hydroxylation, N-dealkylation, and conjugation with glutathione (Ashton and Crafts, 1981; Lamoureux et al., 1973). Several weed species are resistant to s-triazines because of enhanced metabolism (Gronwald et al., 1989; Le Baron, 1991). The reduced rates of photosynthesis associated with site of action mutants is not present in these metabolic- resistant populations.

4. s-Triazine Herbicide-Resistant Crops

a. Traditional Plant Breeding s-Triazine resistance ( pshA gene mutant) has been incorporated into several crops. Hybridization methods have been used to transfer this type of resistance from weedy bird’s-rape (B. campestris) (Beversdorf et al., 1980); to rutabaga and rapeseed (Beversdorf and Hume, 1984), as well as from weedy green foxtail (S. viridis, subspp. viridis Briquet) to foxtail millet (S. viridis, subspp. italica Bri- quet) (Darmency and Pernes, 1989). Agronomic performance has in many cases been less in the resistant crop compared to that in the susceptible crop (Beversdorf eta/., 1988; Dekker, 1983).

b. Biotechnological Techniques s-Triazine-resistant crops have been developed utilizing tissue culture selection and protoplast fusion techniques. Tissue culture selection has led to resistant tobacco (mutant D-1; Pay et al., 1988; Rey et nl., 1990) and potato (mutant D-I; Smeda et al., 1989) HRCs. Protoplast fusion transfer of the psbA gene to potato was accomplished with a weedy relative as the source of resistance (Gressel et al., 1990). Protoplast fusion methodologies were also used to incorporate s-triazine resistance in rapeseed and in several other Brassica species, including broccoli (B. oleracene, var. italica; Christey et al., 1991). 84 J. DEKKER AND S. 0. DUKE

Three triazine-resistant canola cultivars have been released in Canada (cv. ‘OAC Triton,’ “OAC Tribute,” and “OAC Triumph”) with little commercial success. Farmers have generally only used these cultivars when they were willing to trade a significant yield and quality reduction for control of weeds that could be managed with triazine herbicides better than with other methods (Duke et al., 1991; Hall et al., 1995). Efforts to produce cultivars with triazine resistance and normal photosynthetic productivity have been unsuccessful (Hall et al., 1995).

B. ACETOLACTATESYNTHATASE INHIBITORS

1. Introduction

Three groups of herbicides whose site of action is acetolactate synthatase (ALS) are either available or soon will be. They are the sulfonylureas, imidazolinones, and the triazolopyrimidine sulfonanilides (Devine et al., 1993a; Hawkes et al., 1989). Reviews are available on the sulfonylureas (Beyer et al., 1988) and tri- azolopyrimidines (Subramanian and Gerwick, 1989), and an entire book is available on the imidazolinones (Shaner and O’Connor, 1991). Compounds from other chemical families that act at this site are under development. ALS inhibitors are generally highly active and selective and are used for both soil-applied and postemergence weed management. Particular compounds have been designed with particular crops in mind. Thus, certain ALS inhibitors are favored for each crop, resulting in the marketing of a relatively large and growing number of ALS inhibitor herbicides. Examples of sulfonylureas include bensulfuron methyl, chlorsulfuron, nicosulfuron, sulfometuron, and primsulfuron. The imidazolinones include imazaquin, imazapyr, and imazethapyr, and the newer triazolopyrimidine sulfonanilides are represented by flumetsulam.

2. Modes of Action and Resistance

ALS (also known as acetohydroxy acid synthase or AHAS) is the first enzyme in the branched chain amino acid pathway that produces valine, leucine, and isoleucine (Devine er al., 1993a). This enzyme and others in the pathway are found only in the plastid. It is nuclear encoded and, thus, requires a transit sequence to be properly imported and processed. A large number of compounds have been found to be effective inhibitors of ALS, apparently binding a vestigal ubiquinone- binding site (Schloss et ul., 1988). In many ways the herbicide-binding site of ALS is similar to the herbicide-binding site of D-1 of PS I1 (see the section on triazine). The ALS inhibitor herbicides stop growth and then kill the plant relatively HERBICIDE-RESISTANTFIELD CROPS 85 slowly compared to some of the older contact herbicides. Their mechanism of action was discovered by studies in which the effects of the herbicide could be prevented by feeding cell cultures leuine, valine, and isoleucine. ALS appears to be a particularly good molecular target site for herbicides, considering how little of the best ALS inhibitors is needed to kill plants. Only a few grams per hectare of certain sulfonylureas are needed to kill target weeds. Crops that are naturally unaffected by these compounds are resistant due to rapid metabolic degradation of the herbicide (Beyer et al., 1988; Shaner and Mal- lipudi, 199 l). However, weeds that have evolved resistance to ALS inhibitors almost always have evolved an ALS that is resistant to the herbicide (Devine et al., 1993, Chapter 13; Schmitzer et al., 1993). Within the same species, every sort of cross-resistance pattern imaginable seems possible with ALS herbicide resistance, whether selected in tissue culture or in the field. As with the D-1 protein of PS 11, there appear to be various herbicide-binding domains on ALS, which can overlap to provide cross-resistance (Mourad and King, 1992). Cross-resistance can be due to a single mutation or to combined mutations, each conferring resistance to only one ALS inhibitor class (Hattori et al., 1992). There are at least 10 mutation sites in the ALS-encoding gene that confer herbicide resistance without compromising enzyme activity (Mazur and Falco, 1989). Resistance evolves comparatively rapidly to ALS inhibitor herbicides compared to other herbicides. Resistance has appeared in weed populations in only 3 to 5 years of selection with sulfonylureas (Thill et al., 1991) and imidazolinones (Schmitzer et al., 1993). Some sulfonylurea herbicide-resistant weed biotypes may have some altered physiological characteristics (Dyer et al., 1993a; Alcoer- Ruthling et al., 1992); however, it is not clear as to whether this affects fitness. The ALS enzyme efficiency is not significantly affected by most of the mutations that result in resistance. This may be due largely to the fact that the herbicide- binding site is different from the active site of the enzyme. From the large number of good inhibitors and the different types of mutations conferring different patterns of cross-resistance to different ALS inhibitors, one can infer that the herbicide-binding site of ALS is a very plastic molecular domain. X-ray crystal- lography studies have not yet been conducted with ALS, so an accurate description of the binding site remains to be elucidated.

3. ALS Inhibitor-Resistant Crops

Both sulfonylurea- and imidazolinone-resistant crops have been produced. It has been relatively easy to tailor these herbicides to specific crops that metabolically degrade them. It has also been quite easy to generate crops resistant to ALS inhibitors that lack natural resistance. Because of the plasticity of the enzyme, selection out at the seed or whole plant (e.g., Sebastian et al., 1989), organ (e.g., 86 J. DEKKER AND S. 0.DUKE

Harms et a/., 1991), and tissue or cellular level (e.g., Hart et al., 1993) has been a very simple and successful strategy to produce such crops. At the whole plant level, mutagens have proven helpful in providing sufficient genetic diversity.

a. Sulfonylureas The topic of sulfonylurea-resistant crops has been specifically reviewed previously (Saari and Mauvais, 1994). In only one case has sulfonylurea herbicide resistance been transferred from a evolved resistant weed (prickly lettuce; Mallory- Smith et al., 1991) to a crop (lettuce) by conventional breeding methods (Mallory-Smith et al., 1993). Mutant selection has created sulfonylurea herbicide-resistant lines of barley (Baillie et al., 1993), tobacco (Chaleff and Ray, 1984), canola (Tonnemaker et al., 1992), sugarbeet (Hart et al., 1993; Saunders et al., 1992), soybean (Sebastian et al., 1989), rice (Terakawa and Wakasa, 1992), and flax (Jordan and McHughen, 1987), as well as some horticultural crops. The trait is always a single gene mutation and is usually inherited as a semidominant or dominant trait. Almost all mutants selected are resistant because of resistant ALS, although resistant mutants without resistant ALS have been selected once (Sebastian and Chaleff, 1987) and a partially resistant ALS that was amplified was found in another case (Harms et al., 1992). Genetic engineering has produced sulfonylurea-resistant crops (Falco et al., 1989). Arabidopsis thaliana chlorsulfuron-resistant ALS has been transferred to chicory (Vermeulen et al., 1992), tobacco (Gabard et al., 1989), poplar (Brasileiro et al., 1992), canola (Brassica napus; Miki et al., 1990), flax (McSheffrey et al., 1992), and rice (Li et al., 1992). A mutant tobacco ALS has been used to transform cotton (Saari and Mauvais, 1994) and sugarbeet (D’Halluin et al., 1992), and a resistant maize ALS has been used to transform maize (Fromm et al., 1990). Several field tests of sulfonylurea-resistantcrops created by biotechnology have been reported. Transgenic flax expressing a resistant ALS was as productive as untransformed varieties (McHughen and Holm, 1991; McSheffrey et al., 1992) whereas, in the absence of the herbicide, there appeared to be a yield penalty in lines of tobacco transformed with a resistant ALS (Brandle and Miki, 1993). A rapeseed line derived by selection in cell culture was less productive, and produced harvestable seed later, than the wild type (Magha et al., 1993). Because of the large number of available sulfonylureas for most crops, there is not as much interest in creating crops resistant to them as there is in creating crops resistant to other herbicides.

b. Imidazolinones The topic of imidazolinone-resistant crops has been reviewed previously by Newhouse er al. (199 1b) and Shaner et al. (1994). The first imidazolinones reg- istered for use in the United States, imazaquin and imazethepyr, were used in HERBICIDE-RESISTANTFIELD CROPS 87

soybeans. These herbicides are very effective on many of the problematic weeds in maize, but maize is susceptible. Furthermore, maize is often planted in rotation with soybeans so that residual imidazolinone herbicides can cause crop damage. Selection for imidazolinone-resistant maize began in 1982 (Shaner et al., 1994). Imidazolinone resistance was sucessfully selected for in tissue culture (Newhouse era/., 1991b) and by pollen mutagenesis (Shaner eta/., 1994) to produce imidazolinone-resistant maize. Maize seed with this trait is the only commercially available herbicide-resistant crop in the United States at this writing. Work is in progress to produce imidazolinone-resistant wheat (Newhouse eta/., 1992) and canola (Swanson et al., 1988, 1989). Initial field data confirm that both imidazolinone-resistant canola and wheat have the same yield as susceptible varieties in the absence of the herbicide and that the selected varieties are resistant to rates of imidazolinones recommended for weed control (Shaner et al., 1994). Commercial varieties of imidazolinone-resistant wheat and canola are expected to be available in the late 1990s.

C. ACETYL-COACARBOXYLASE INHIBITORS

1. Introduction

This group of herbicides includes the aryloxyphenoxypropionates and the cyclohexanediones (Devine et al., 1993a; Duke and Kenyon, 1988). Some commonly used aryloxyphenoxypropionates are diclofop, haloxyfop, and fluazifop and some commercial cyclohexanediones are sethoxydim and alloxydim. Hence, some people refer to the two herbicide classes as the “fops” and “dims.” Both herbicide classes are postemergence grass killers that are used extensively in agronomic crops. Although chemically different, they both target the same molecular site and produce similar effects on grass weeds. They are generally active at lower rates than many older herbicides (e.g., atrazine).

2. Modes of Action and Resistance

The ACCase form inhibited by herbicides is a plastid-localized enzyme that catalyzes ATP-dependent carboxylation of acetyl-CoA to form malonyl-CoA in the lipid synthesis pathway of plants. ACCase is a pivotal enzyme in the plant lipid biosynthesis pathway, exerting strong flux control, especially in light-stimulated biosynthesis (Page el al., 1994). Another cytosolic form of ACCase is not inhibited by herbicides and apparently plays no role in their mode of action (Egli et al., 1993). Both aryloxyphenoxypropionates and cyclohexanediones strongly inhibit ACCase, and this enzyme appears to the the primary site of action for these herbicides (Devine et a[., 1993a; Harwood, 1991). 88 J. DEKKER AND S. 0. DUKE

A direct effect on membrane function has been proposed as a site of action of these herbicides (Shimabukuro and Hoffer, 1992); however, the action at this site does not appear to kill plants at herbicidal doses (DiTomaso et al., 199 1 ; Dotray et al., 1993). The membrane effect appears to be antagonism of auxin-stimulated proton effux at the receptor level (Barnwell and Cobb, 1993). Auxin antagonism of these compounds has been known since they were first discovered (Duke and Kenyon, 1988). Wild oat with resistance to diclofop and fenoxaprop, two ACCase inhibitor herbicides, had neither enhanced herbicide degradation nor resistant ACCase, but was able to reverse herbicide effects on transmembrane proton fluxes (Devine et al., 1993b). Crop resistance to these herbicides appears to normally be due to an insensitive ACCase (Burton et al., 1987; Devine et al., 1993a). Some grasses such as wheat are resistant to some of these herbicides because they can metabolically degrade them rapidly (Shimabukuro, 1990). Red fescue is naturally resistant by virtue of a herbicide-resistant ACCase (Stoltenberg et al., 1989). Weeds appear to have evolved at least three different mechanisms of escaping the phytotoxicity of members of this herbicide group. Some biotypes have evolved a herbicide-resistant ACCase (e.g., Marles et al., 1993; Tardiff et al., 1993). Oth- ers appear to more rapidly degrade certain ACCase inhibitors (Kemp et al., 1990), although this has not yet been rigorously proven. In at least one case, the resistance appears to be due to an altered membrane response (Devine et al., 1993b).

3. ACCase-Resistant Crops

Maize resistant to both arylox yphenoxypropionates and cyclohexanediones has been produced by selection for mutations conferring resistance in tissue culture and then regenerating the plant (Marshall et al., 1992; Parker et al., 1990a,b; Somers, 1994). This approach has also been used to select for herbicide-resistant wheat and Kentucky bluegrass (Somers, 1994), although these efforts have not yet been well documented or have been unsuccessful. Several types of mutations have been generated, as characterized by varying degrees of cross-resistance to ACCase inhibitors not used for selection of the mutant. For example, the maize mutants Acc 1-S 1, Acc 1-S2, and Acc-S3 are resistant to both sethoxydim and haloxyfop, whereas the Acc I -H 1 mutant is resistant to only haloxyfop, and the Accl-H2 mutant is very resistant to haloxyfop, but only partially resistant to sethoxydim (Marshall er al., 1992). In the absence of herbicides, ACCase levels in the S lines are similar to the wild type and those of the H lines are only slightly lower. Whole plant resistance of several mutant lines closely parallels the ACCase resistance (Somers, 1994). Field trials with sethoxydim-resistant maize have demonstrated that no injury occurs to the crop at 0.88 kgha of sethoxydim, a rate in excess of that required to control grassy weeds (Dotray et al., 1992). Herbicide treatment had no adverse HERBICIDE-RESISTANT FIELD CROPS 89 effects on grain yield or quality. The germ plasm for resistance to ACCase- inhibiting herbicides was transferred to commercial maize breedingcompanies in 1990, and backcrossing and inbred development are in progress (Somers, 1994).

D. GLYPHOSATE

I. Introduction

Glyphosate [(N-phosphonomethyl)glycine] is the only herbicide in its class. The physical and biological characteristics of glyphosate have been reviewed (Duke, 1988) and an entire book has been devoted to this one compound (Gross- bard and Atkinson, 1985). Glyphosate is a nonselective, postemergence herbicide that is used extensively prior to crop emergence, as a harvest aid, and as a directed spray. It is used extensively in forests and orchards where understory vegetation can be sprayed without contacting the foliage of the crop. It is also used in land- scaping and lawns for edging and borders. Very few weeds are resistant to glyphosate and there are no reported cases of evolved resistance. It is toxicologically and environmentally benign (Duke, 1988). Upon contact with the soil, it is immobilized by binding to soil components, where is it is rapidly degraded by soil microbes.

2. Modes of Action

Glyphosate is normally a slow-acting herbicide that can take several days to weeks to kill a plant. It is translocated readily from sites of uptake (normally foliage) to metabolic sinks, such as meristems, developing leaves, and storage organs (Duke, 1988). Most plants do not metabolically degrade glyphosate. The shikimate pathway and, more specifically, the EPSPS is the primary site of action of the herbicide. EPSPS is a nuclear-coded, plastid enzyme. The shikimate pathway is the biosynthetic source of the three aromatic amino acids: phenylala- nine, tryptophan, and tyrosine. These amino acids are necessary for protein synthesis as well as for biosynthesis of auxin, most plant phenolic compounds, and other secondary compounds. Furthermore, blockage of the shikimate pathway at EPSPS leads to deregulation of the pathway, resulting in accumulation of huge, possibly phytotoxic, concentrations of shikimate and benzoic acid derivatives of shikimate (Lydon and Duke, 1988). This deregulation and enhanced carbon flow into the shikimate pathway drains other biosynthetic pathways of necessary build- ing blocks (Killmer et al., 1981; Jenson, 1985). Thus, the blockage of the shikimate pathway can lead to a large number of potentially damaging physiological effects. There is no good evidence of any other primary site of action of glyphosate (Duke, 1988), although very rapid effects of glyphosate on photosynthesis in 90 J. DEKKERAND S. 0. DUKE some species are difficult to explain by an effect on EPSPS (Madsen er al., 1995; Sheih et af., 1991). Designing HRCs around a single target site by site modification requires that no other sites of action can play a significant role in phytotoxicity under any field conditions. No plants are considered to be naturally resistant to glyphosate, although there is considerable variation in sensitivity. The physiological bases for these varia- tions in susceptibility are poorly understood.

3. Glyphosate-Resistant Crops

The production of glyphosate-resistant crops has been the focus of much research for over a decade. A major problem in the production of glyphosate- resistant plants is that its glyphosate is readily translocated to rneristems and other metabolic sinks where it is concentrated to levels many times that found in leaves. Furthermore, it is not metabolically degraded to a significant extent. So, although the plant may be resistant at the foliar level, the concentrations that accumulate in meristems, flower buds, and other metabolic sinks may overwhelm the resistance mechanism. Even if this is not the case, unacceptable residues of the herbicide might accumulate in the harvested portions of the plant. Overcoming these problems has slowed the development and introduction of glyphosate-resistant crops. Research to produce glyphosate-resistant crops has gone through three phases. The first approach was to select for glyphosate resistance in tissue or cell culture and then to regenerate glyphosate-resistant plants from resistant cells or tissues by selection on glyphosate-containing media. The resulting selections were generally found to have more EPSPS than the wild type due to gene amplification (e.g., Goldsbrough et af., 1990; Shah er al., 1986); however, the EPSPS was equally susceptible to glyphosate as the wild type. The amplification is generally stable in the absence of the herbicide, and plants regenerated from cell cultures with amplified EPSPS maintain amplified EPSPS genes (Shyr et af., 1992; Wang el al., 1991). Amplification of EPSPS can occur at the gene, mRNA (enhanced transcription), or enzyme (reduced turnover) levels (Hollander-Czytko et af., 1992). Glyphosate is simply diluted by a larger number of enzyme molecules. The level of resistance obtained by this approach was not useful for commercial application. In at least one case, selection with glyphosate in cell cultures resulted in resistance due to a glyphosate-resistant EPSPS. Forlani et al. (1992) selected maize cell cultures with glyphosate and produced a cell line with a glyphosate-resistant EPSPS. However, the cell line still had a tolerant form of EPSPS and the resistant form had reduced enzymatic efficiency, thus making it of no commercial value. The second approach to the generation of glyphosate-resistant crops has been to transform them with genes encoding glyphosate-resistant EPSPS. Several HERBICIDE-RESISTANTFIELD CROPS 91

EPSPSs have been produced with reduced sensitivity to glyphosate (Padgette et al., 1991; Sost and Amrhein, 1990; Stalker et al., 1985); however, these forms of EPSPS are generally less efficient than the wild type, resulting in unacceptable pleiotropic effects unless the level of the inefficient but resistant EPSPS is increased. Initial attempts to transform plants with resistant EPSPS were also hampered by the fact that no transit peptide to target the gene product to the plastid was included (Comai et al., 1985; Fillati et al., 1987). These plants were only slightly resistant to glyphosate. The introduction of a chloroplast transit signal improved the level of resistance (Della-Cioppa et al., 1987). An EPSPS from strain CP4 of Agrobacterium sp. was found with a high level of glyphosate insensitivity and good enzymatic efficiency (Barry et af., 1992). Plants transformed with the gene encoding this enzyme, along with a chloroplast transit peptide to target the enzyme for the plastid, resulted in highly resistant canola and soybean. The leading transgenic glyphosate-resistant soybean line ex- presses the CP4 EPSPS (Padgette et al., 1994). There appears to be no yield penalty from this gene and it confers a high level of glyphosate resistance. The third and most recent approach to glyphosate-resistant crops has been to introduce genes from microbes that degrade glyphosate. Plants do not generally degrade glyphosate and no plant enzyme has been found to have such activity. However, many soil microbes readily degrade glyphosate. Certain species of Pseudomonas and other soil microbes convert glyphosate to sarcosine and PPi with a C-P lyase activity (e.g., Kishore and Jacob, 1987). The enzyme itself has not been isolated and despite good progress in understanding the molecular ge- netics of C-P lyase, this enzyme was abandoned because of the complexity and number of gene products (Barry et al., 1992). The predominant degradation pathway in soil appears to be an initial conversion of glyphosate to aminomethylphos- phonic acid (AMPA) and glyoxylate (Tortensson, 1985). Although this enzyme has not been isolated, the gene from an Achromobacter sp. strain taken from a glyphosate waste stream treatment facility has been cloned and used to transform crops (Barry et al., 1992). A region from the DNA of this microbe encodes glyphosate oxidoreductase (COX) which cleaves the C-N bond of glyphosate, producing AMPA and glyoxylate. Expression of COX in plants imparts glyphosate resistance, and targeting GOX for the plastid with a chloroplast transit peptide improves the level of resistance (Barry et al., 1992; Padgette et al., 1994). At this writing, there are no published accounts of weed management experi- ments with glyphosate-resistant crops. However, Madsen and Jensen (1 995) found that with glyphosate-resistant sugarbeets, glyphosate alone in three applications (720 g a.i./ha total) was just as effective as a conventional application of 4 kg a.i.1 ha of other herbicides (phenmedipham, ethofumesate, and metamitron) applied in three sprayings. 92 J. DEKKER AND S. 0. DUKE

E. BROMOXYNIL

1. Introduction

Bromoxynil is a postemergence benzonitrile herbicide used on barley, oats, wheat, flax, rice, and in grass seed production. Dicotyledonous crops are especially sensitive to bromoxynil and, thus, the generation of a dicotyledonous bromoxynil-resistant crop would extend its use, especially in crops such as cotton for which there are presently no good postemergence herbicide options. A related nitrile herbicide, ioxynil, is also commercially available. Bromoxynil is a relatively short-lived herbicide, with a soil half-life as short as 1 week, due to microbial degradation (Stalker et al., 1994).

2. Modes of Action and Resistance

Bromoxynil is a photosystem I1 inhibitor with the same mode of action as triazines (see earlier discussion) (Devine et al., 1993a). The crops with which bromoxynil is used are apparently naturally resistant through rapid metabolic degradation of the herbicide (Ashton and Crafts, 1981; Schaller et al., 1991, 1992), although this is not a well-studied topic. Bromoxynil-resistant weeds have been reported (LeBaron, 1991), although the mechanism of resistance has not. In some cases, resistance to triazine herbicides can impart greater susceptibility to bromoxynil; a case of negative cross-resistance (Durner et al., 1986). Thus, bromoxynil could be useful in managing triazine-resistant weeds.

3. Bromoxynil-Resistant Crops

Bromoxynil-resistant tobacco and cotton have been generated by transformation with a plasmid gene from the bacterium Klebsiella ozaenae that encodes a bromoxynil nitrilase enzyme (Stalker et al., 1988a,b, 1994). Resulting plants are resistant to up to 10-fold the recommended field rates of commercial formulations of bromoxynil. In cotton, the gene was introduced via Agrobacterium and was expressed as a dominant Mendelian gene. At rates up to 1 1.2 kg a.i./ha (0.56 kg a.i./ha is a normal field rate), no phytotoxicity to the transgenic cotton varieties is seen. Metabolic studies have shown that all of the bromoxynil is converted to non- phytotoxic degradation products in bromoxynil-resistant cotton, whereas more than 99% of the bromoxynil extracted from susceptible, nontransformed cotton remained as bromoxynil (Stalker et al., 1994). Bromoxynil-resistant cotton may be the first transgenic herbicide-resistant crop introduced to the market. It has been successfully tested throughout the cotton- HERBICIDE-RESISTANT FIELD CROPS 93

growing areas of the United States, except California (e.g., Arkansas, Beaty and Guy, 1994; South Carolina, Murdock, 1994; Georgia, Richburg el al., 1993). No undesirable pleiotropic effects of the nitrilase gene have been noted. Bromoxynil- resistant cotton was approved by the U.S. Department of Agriculture in 1994; however, at this writing it still awaits clearance by the U.S. Food and Drug Admin- istration and the U.S. Environmental Protection Agency.

F. PHENOXYCARBOXYLICACIDS (E.G., 2,4-D)

1. Introduction

The phenoxycarboxylic acids (PCAs) such as 2,4-D and 2,4,5-T are among the oldest synthetic herbiciges. These compounds are used primarily for postemergence management of dicot weeds in grass crops, pastures, forests, and lawns. The butryric acid derivative of 2,4-D, 2,4-DB is a proherbicide (a herbicide that is inactive in the form applied) that is metabolized to 2,4-D in sensitive species. Some legumes that are sensitive to 2,4-D are tolerant to 2,4-DB because they lack the P-oxidation activity required to activate it. Phenoxycarboxylic acids have been off patent for many years and are very effective and inexpensive. Sensitive crops and ornamentals are often injured by 2,4-D spray drift from applications to tolerant crops or turf. Introduction of 2P-D-resistant crops could eliminate damage to these crops from such a source-the purported or implied objective of some research to generate 2,4-D-resistant cotton (Bayley et af., 1992; Lyon et al., 1993). This herbicide would be extremely useful and cost effective as a postemergence herbicide in cotton, a crop for which there is presently no ade- quate foliar-applied herbicide.

2. Modes of Action and Resistance

Despite many years of study the actual molecular site of action of this family of herbicides is unknown. The PCAs are sometimes called hormone-type herbicides because they mimic in many ways lethal doses of the plant hormone indole- acetic acid (IAA) (Devine et af., 1993a). IAA and the PCAs are both thought to act by influencing plasma membrane properties by acting at a molecular site in the plasma membrane. Resistance of grasses to these herbicides appears to be related to rapid metabolic conversion to irreversible products, whereas in dicotyledonous species the herbicide is often found in the form of reversible conjugates (Devine et af., 1993a,b). Several weed species have evolved resistance to 2,4-D (LeBaron, 1991). Where studied, the resistance appears to be due to metabolic detoxification. 94 J. DEKKER AND S. 0. DUKE

3. 2,4-D-Resistant Crops

The half-life of 2,4-D in soil is relatively short, due to several microbes that readily degrade it (Llewellyn and Last, 1994). Certain Alcaligenes eutrophus (a bacterium) strains contain a large plasmid (75 kb) containing genes for enzymes that fully degrade 2,4-D. The first step in the enzymatic degradation of 2,4-D is its oxidation to dichlorophenol (DCP) by a dioxygenase encoded by the tfdA gene. DCP is 50- to 100-fold less phytotoxic than 2,4-D (Llewellyn et al., 1990), so the gene encoding this dioxygenase is apparently the only gene needed to confer resistance to crops. There has been some concern about the safety of DCP as a food residue in 2,4-D-resistant crops. The latter genes of the Alcaligenes plasmid 2,4-D degradation pathway have been cloned and sequenced (Perkins et al., 1990) and could be used to provide a more complete degradation of 2,4-D in plants. Cotton and tobacco have been made resistant to 2,4-D by genetic transformation with the tfdA gene (Bayley et al., 1992; Llewellyn and Last, 1994; Lyon et al., 1989, 1993; Streber and Willmitzer, 1989). All three groups who have made these transformants have used the 35s promoter of the cauliflower mosaic virus, in some cases with additional promoters. The resultant transformants are resistant to more than three times the highest recommended doses of 2,4-D for wheat, corn, sorghum, or pasture. In the case of cotton, this represents a 50- to 100-fold increase in tolerance to 2,4-D compared to untransformed controls. Transgenic cotton seed with 2,4-D resistance has been distributed to private and public plant breeders in the United States for possible incorporation into commercial germ plasm (Llewellyn and Last, 1994). In Australia the 2,4-D tolerance gene is currently being transferred to the best commercail cotton varieties with expectations of commercial release as 2,4-D drift-tolerant cultivars by the year 1998 (Lyon et al., 1993).

G. GLLJFOSINATE(PHOSPHINOTHRICIN)

1. Introduction

Glufosinate, the chemically synthesized version of the microbial product (phosphinothricin), is used in Europe and other parts of the world as a nonselective herbicide (Devine et al., 1993a). It is a toxicologically and environmentally benign herbicide that does not persist in the environment. Streptomyces spp. produce phosphinothricin and a precursor of phosphinothricin, bialaphos. Bialaphos can be converted by plants to phosphinothricin, thus generating a phytotoxin. Biala- phos produced in fermentation culture is sold in Japan as a herbicide. These products are foliar-applied, contact herbicides that act faster than gly- HERBICIDE-RESISTANTFIELD CROPS 95

phosate, but slower than paraquat. Although some plant species are more tolerant of glufosinate than others, it is generally used as a nonselective herbicide in much the same way as glyphosate. Resistant crops would greatly increase the utility of this herbicide.

2. Modes of Action and Resistance

Glufosinate is the most potent known inhibitor of glutamine synthetase (GS) (Devine et al., 1993a). GS is critical to the assimilation of nitrogen by plants, and its inhibition leads to several immediate metabolic dysfunctions. Initially, it was thought that most of the phytotoxicity caused by GS inhibitors was due to accumulation of toxic levels of ammonia, a GS substrate. However, it now appears that the rapid cessation of photosynthesis brought about by glyoxylate accumulation is the more important phytotoxic effect. Glyoxylate accumulates in GS-inhibited plants because the levels of amino acids required in photorespiratory glyoxylate transamination are reduced. No weeds have yet evolved resistance to glufosinate. However, this is a relatively new herbicide and it is a contact herbicide with a very short selection pressure duration. There is considerable natural variation between species in sensitivity to glufosinate, and this variation does not appear to be based on differential sensitivity to GS (Ridley and McNally, 1985). Lines of oat that are insensitive to the GS-inhibiting glufosinate analog, tabtoxin, have a tabtoxin-resistant GS iso- zyme (Knight et al., 1988); however, no plants with glufosinate-resistant GS have been reported.

3. Glufosinate-Resistant Crops

Glufosinate-resistant crops have been the focus of at least two reviews (Mullner et al., 1993; Vasil, 1994). Two genes that encode enzymes that metabolically inactive glufosinate have been used to produce resistant plants by transgenic methods. The bar gene from Streptomyces hygroscopicus andlor the pat (phosphinothricin-aceytl transferase) gene from S. viridochromogenes has been used to transform about 20 crops, including carrot (Droge et al., 1992), oats (Somers et al., 1992), beet (Botterman and Leemans, 1988), oilseed rape (De- Block et al., 1989), tall fescue (Wang et al., 1992), barley (Wan and Lemaux, 1994), tomato (DeBlock et al., 1989), alfalfa (D’Halluin et al., 1990), rice, (Cao et al., 1992; Datta et al., 1992; Rathmore et al., 1993), potato (DeBlock et al., 1987), sorghum (Casas et al., 1993), wheat (Vasil et al., 1993), tobacco (Droge et al., 1992), sugarbeet (D’Halluin et al., 1992), and maize (Fromm et al., 1990; Laursen et al., 1994). Both of these similar genes encode a phosphinothricin- acetyl transferase. Sugarcane has been transformed with the pat gene in callus 96 J. DEKKER AND S. 0. DUKE culture, but no plants have yet been regenerated (Chowdhury and Vasil, 1992). The Emu promoter, which drives high levels of gene expression in cereals, works well with the pat gene (Chamberlain et al., 1994). There is apparently no crop yield or quality sacrifice for either of these genes. Comparing glufosinate use with glufosinate-resistant crops with standard weed management methods in agronomic crops, the total volume of herbicides used can be reduced substantially (Mullner et al., 1993). An additional benefit of glufosinate-resistantcrops is that bialaphos and glufosinate are toxic to some pathogens, so the herbicide might also act as a fungicide to protect the crop, as has been found against sheath blight in rice (Uchimiya et al., 1993). Whether the bar or pat genes will also protect against pathogens that produce analogs of glufosinate (e.g., tabtoxin) as virulence factors has not been reported. The risk of out- crossing of transgenic glufosinate-resistant rapeseed has been assessed with the conclusion that the risk for gene dispersal is limited (Kerlan et al., 1992). The bar and pat are used extensively as selectable markers. The advantage of these genes is that the selection agent is inexpensive and highly efficient. Thus, the production of a glufosinate-resistantcrop per se has not always been the major objective of the many published examples (Yoder and Goldsbrough, 1994).

H. OTHERHERBICIDES

1. Cyanamide

Cyanamide is a herbicide used in Europe. Its mode of action and mechanism of selectivity are unknown. Tobacco has been made resistant to cyanamide by transformation with a gene from the fungus Myrothecium verrucaria that encodes cyanamide hydratase (Maier-Greiner et al., 1991), an enzyme that converts the herbicide to urea. Whether this capability will be exploited to expand the use of cyanamide is unknown.

2. Dalapon

Dalapon is a chlorinated aliphatic acid. Its mode of action is unclear, perhaps because it has several molecular sites of action. One of its physiological effects is to inhibit the synthesis of very long chain fatty acids (Devine et al., 1993a,b). Plants do not readily metabolically degrade dalapon (Foy, 1975), and the mechanism of natural resistance is unknown. This herbicide is or has been used extensively as a grass killer in asparagus, citrus, cotton, flax, peas, potatoes, and sugarbeets (Klingman and Ashton, 1982). However, there are several major IIERBICIDE-RESISTANT FIELD CROPS 97 crops with which this relatively inexpensive herbicide cannot be used because of phytotoxicity. Dalapon-resistant tobacco (Nicotinna plurnbaginifolia) has been produced by transgenic methods (Buchanan-Wollaston et a/., 1992). A gene from Pseudo- rnonas putida encoding a dehalogenase capable of degrading dalapon was used in the transformation. Resulting transformants were resistant to five times the recommended field rate of dalapon. This study was not done to generate a commercial herbicide-resistant tobacco, and it is not known if a similar approach will be used to produce dalapon-resistant crops for commercial use.

3. Phytoene Desaturase Inhibitors

Carotenoid synthesis is dependent on phytoene desaturase. Inhibition of this enzyme leads to albino plants because chlorophyll will not accumulate in the absence of carotenoids. Only two phytoene desaturase inhibitors, fluridone and norflurazon, are commercially available, and, of these, only norflurazon is used on the agronomic crop cotton. Diflufenican, another phytoene desaturase inhibitor, is being developed for use in wheat and barley. Norflurazon is generally used as a pre-emergence, soil-applied herbicide. Several important crops are not resistant to it and there is sometimes phytotoxicity to cotton. Furthermore, because of its persistence in soil, phytotoxicity can be experienced the next year in rotated crops. A major problem with phytoene desaturase inhibitors is their lack of selectivity. Thus, the advent of crops with resistance to these herbicides at the phytoene desaturase level would be especially useful. No cases of evolved resistance to these herbicides have been reported. Natural resistance of crops and weeds to these herbicides is not well studied. Metabolic degradation of norflurazon in cotton is not faster than in some susceptible weeds, and there is evidence that sequestration of norflurazon in the lysigenous glands that cover the hypocotyl and cotyledons of cotton imparts tolerance to cotton (Duke, 1992). Glandless cotton varieties are more susceptible to norflurazon than those with glands (Stegink and Vaughn, 1988). Crops that are resistant to phytoene desaturase inhibitors are under development (Sandmann et al.. 1995). A gene from the norflurazon-resistantbacterium Envinia uredovora that encodes a norflurazon-resistant phytoene desaturase has been inserted into tobacco to produce a herbicide-resistant crop (Misawa et al., 1993). The crtl gene of the bacterium was fused with the sequence encoding the plastid transit peptide for pea Rubisco (small subunit) and put under the control of the cauliflower mosaic virus 35s promoter. This construct was inserted via Agrobac- teriurn. Resistance was dominantly inherited. Cross-resistance to several other phytoene desaturase-inhibiting herbicides was expressed. Using a naturally resistant gene product instead of one that has been selected 98 J. DEKKER AND S. 0.DUKE for may increase the odds of the gene product being highly functional without pleiotrophic effects due to impaired catalytic function. Whether the success with tobacco will spur development of herbicide-resistant crops for use with phytoene desaturase inhibitor herbicides is an open question.

4. Protoporphyrinogen-Oxidase(Protox) Inhibitors

One of the most patented groups of herbicides in recent years are the inhibitors of Protox (Anderson et al., 1994). Commercialized herbicides with this molecular site of action include acifluorfen, lactofen, oxadiazon, and fomesafen. These herbicides are contact herbicides that are applied as foliar sprays which cause very rapid cellular collapse and desiccation. The most effective of these compounds can be used at rates of only a few grams per hectare. One of the major problems with this group of herbicides is that only a few crops (primarily soybean and rice) Protox is the last enzyme in the porphyrin pathway that is common to both heme and chlorophyll synthesis pathways. These compounds cause massive levels of the enzyme product (not the substrate) protoporphyrin IX (Proto IX) to accumulate through a complex mechanism involving both a herbicide-susceptible chloroplast Protox and a herbicide-resistant extraplastidic Proto IX-oxidizing enzyme (Jacobs ef al., 1991; Jacobs and Jacobs, 1993; Lee et al., 1993; Nandihalli and Duke, 1993; Duke et al., 1994). Proto IX is a photosensitizing agent, generating highly reactive singlet oxygen in the presence of sunlight. Thus, Proto IX, a metabolic intermediate, is the acutely toxic agent causing phytotoxicity. There is a wide range in the natural resistance of crops and weeds to these compounds (Sherman et al., 1991; Matsumoto et al., 1994); however, there is no evidence that any weeds have become resistant to these herbicides as the result of selection pressure. There are apparently several mechanisms of resistance, including reduced sensitivity of Protox, metabolic rapid degradation of the herbicide, and resistance to singlet oxygen. Efforts are being made to produce a plant with a herbicide-resistant chloroplast Protox by either selection with Protox inhibitors (Che et al., 1993) or introduction of a resistant Protox from another organism (Sato et al., 1994). The ultimate prac- tical result of this research would be the production of new crops resistant to Pro- tox inhibitors.

5. Bipyridiliums

This group of nonselective herbicides includes paraquat and diquat. Bipyridi- liums are contact herbicides that cause very rapid desiccation of foliage. They are the fastest acting group of herbicides. They are acutely toxic to animals. These herbicides kill green plants by accepting an excited electron from photosystem I of photosynthesis to form the paraquat radical, which in turn gen- HERBICIDE-RESISTANTFIELD CROPS 99

erates a highly destructive superoxide radical (Devine et al., 1993a). The paraquat radical is formed more slowly in animals through other mechanisms. Some weeds have become resistant to paraquat; however, the mechanism of resistance is in dispute. One group has evidence that paraquat resistance is due to greater expression of existing genes encoding enzymes that protect against superoxide and its peroxidizing products (e.g., Amsellem et al., 1993). The other view is that the resistant biotypes have evolved a mechanism to exclude paraquat from the molecular site of action (e.g., Norman et al., 1993). Paraquat-resistant crops have been produced by increasing protective enzyme levels by transgenic means. An E. coli gene encoding glutathione reductase when inserted into tobacco increased its resistance to paraquat (Aono et al., 1993). Genes for tomato superoxide dismutases transferred potato by use of Agrobacte- rium conferred enhanced tolerance to paraquat (Per1 et al., 1993). The gene from pea for Cu/Zn chloroplast superoxide dismutase imparted paraquat resistance to genetically engineered tobacco (Sen Gupta et al., 1993). These studies were done for purely academic reasons and it is unlikely that paraquat-resistant crops will be introduced. It is possible, however, that such modifications in crops will be used to prevent other types of oxidative stress, such as that caused by ozone or sulfur dioxide (Herouart et al., 1993; Tanaka, 1994).

6. Dihydropteroate Synthase Inhibitors

Asulam is a broad spectrum herbicide that is chemically related to sulfonamide antibiotics. Asulam inhibits folate synthesis by inhibition of dihydropteroate synthase (DHPS) and thereby acts as a herbicide (Devine eta!., 1993a). Some bacte- ria have DHPS that is resistant to sulfonamide antibiotics (Wise and Abou-Donia, 1985). The gene for this enzyme has been fused with a plastid transit peptide sequence and has been used to transform tobacco leaf explants to produce asulam- resistant plants (Guerineau et al.. 1990). Whether there will be any commercial development of this capability is not known. Also, whether this strategy will confer sufficient resistance for commercial use is not known, as asulam is also reported to be a plant mitotic inhibitor (Devine et al., 1993a).

7. Mitotic Inhibitors

Several families of herbicides appear to have a primary effect on molecules involved in cell division (see Devine et al., 1993a). The dinitroanilines apparently bind to the protein subunit of microtubules, tubulin, to disrupt proper assembly of the microtubules required for cell division. Trifluralin, the most widely used dinitroaniline, is used as a preplant incorporated herbicide to control primarily grasses in broadleaf crops such as soybeans and cotton. It has been used for several years and some weed species such as 100 J. DEKKER AND S. 0. DUKE goosegrass have evolved resistance (LeBaron, 199 1). Resistance in goosegrass is apparently due to a modified tubulin (Vaughn and Vaughan, 1990). Some species with natural tolerance to trifluralin, such as carrot, apparently owe their immunity to a modified tubulin, much like that found in resistant goosegrass (Vaughan and Vaughn, 1988). A patent for the production of trifluralin-resistant crops by genetically engineering with a gene encoding the modified tubulin of trifluralin-resistant goosegrass has been filed (Cronin er al., 1993). Whether such crops will be produced and developed is not known.

v. SUMMARY

As a summary of current efforts in the development of HRCs, a list of herbicides and their resistant crops are provided in Table I. Resistant crops are listed

Table I Herbicides and Their Resistant Crops

Herbicide group Herbicide Resistant crops

AlSase inhibitors Sulfonylureas Barley; chicory; cotton; flax; lettuce; maize; poplar; rapeseed; rice; soybean; sugar beet; tobacco Imidazolinones Maize; rapeseed; wheat ACCase inhibitors Kentucky bluegrass; maize; wheat Bipyridiliums Potato; tobacco DHPS inhibitors Tobacco Phenoxycarboxylic acids Cotton; tobacco Phytoene desaturase inhibitors Tobacco Triazines Foxtail millet (Setaria ifnl- icn); potato; rapeseed; rutabaga; tobacco Bromoxynil Cotton; tobacco Cyanamide Tobacco Dalapon Tobacco Glufosinate Alfalfa; barley; beet; carrot; maize; oats; potato; rapeseed; rice; sorghum; sugar beet; tall fescue; tobacco; tomato; wheat GI yphosate Maize; rapeseed; soybean HERBICIDE-RESISTANTFIELD CROPS 101 regardless of whether they have been commercialized or were developed for experimental purposes only, and are provided regardless of their “success” as resistant plants. They are listed whether their development is complete or research is still in progress. In most cases, literature citations for these HRCs have been provided in the text.

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