Annu. Rev. Plant Physiol. Plant Mol. Bioi. 1993.44:203-29 Copyright © 1993 by Annual Reviews 1nc. All rights reserved

MECHANISMS AND AGRONOMIC

ASPECTS OF HERBICIDE

RESISTANCE

Jodie S. Holt

Department of Botany and Plant Sciences, University of California, Riverside, California

92521

Steven B. Powles and Joseph A. M. Holtum

Department of Crop Protection, Waite Agricultural Research Institute, Glen Osmond,

South Australia 5064

KEYWORDS: weed resistance. crop resistance. herbicide target site

CONTENTS

INTRODUCTION ..................................................................................................................... 204

RESISTANCE TO AMINO ACID SYNTHESIS INHIBITORS .. . . .... ............................ ... ...... 204 Acetolactate Synthase (ALS) Inhibitors ....................................... .... . . ... ............. 204 5-En

(?Jl;uh;;;��:j.��'!::����.�.����������.��.�.��.���.�������.��.�!.�.����� ............... 207

Glu tamine Synthetase (GS) Inhibitors ................................... ... . ...... ........ .......... 208

RESISTANCE TO PHOTOSYSTEM II (PSII) INHIBITORS... . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 208

RESISTANCE TO LIPID SYNTHESIS INHIBITORS .. . ............................. ... ... ... ... ........ ....... 211 Acetyl Coenzyme A Carboxylase (ACCase) Inhibitors ..................................... . 211

RESISTANCE TO AUXIN-TYPE HERBICIDES ................ ................................................... 213 Phenoxyacetic Acids ......... .. ... ... ..... ,................................................................... 213

RESISTANCE TO MITOTIC INHIBITORS ....................... ....................................... ... ... ... ... . 215 Dinitroanilines . . . . .. .... . . . . . . .. ... .. . .. ......... .. .. ...... .......... ............................................ 215

RESISTANCE TO PHOTOSYSTEM I (PSI) INHIBITORS ................................................... 217 Bipyridiliums...................................................................................................... 217

CROSS- AND MULTIPLE-HERBICIDE RESISTANCE ....................................................... 219

AGRONOMIC IMPLICATIONS OF HERBICIDE RESISTANCE ........ ............... ...... ........... 221

0066-4294/93/0601-0203$02.00 203

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204 HOLTET AL

INTRODUCTION

The use of herbicides for the last 40 years has selected for increased resistance within formerly susceptible species. The incidence of resistance, fIrst reported in 1970 (99, 143), has risen dramatically over the past 10 years and has been reviewed accordingly (25, 51, 57, 81, 82, 99, 123, 142). To date at least 57 weed species, including 40 dicots and 17 monocots, have evolved resistance to triazine herbicides (Table 1). In addition, at least 60 species have biotypes resistant to one or more herbicides from 14 other herbicide classes (81, 98, and authors' unpublished data). The herbicide classes against which resistance is most common tend to have single target sites under the control of single or very few genes (16). Where the genetics of evolved weed resistance has been studied, one or very few genes are involved (78, 88, 129).

Here we review herbicide resistance in weeds and crops with emphasis on recent insights into mechanisms and agronomic implications. We include brief discussions of engineered resistance in crops (reviewed in this series in 1989: 113; see also 17, 45, 127). Population biology and the evolution of weed resistance were reviewed in 1991 (183) and are dealt with only briefly here. A few herbicides listed in Table 1 as showing resistance are not discussed further

owing to paucity of cases or lack of documentation on the resistance mecha­nism. We include a discussion of herbicide cross- and multiple-resistance, the most serious recent developments in weed resistance (136, 137).

Resistance denotes the ability of a population of plants within a species or larger taxonomic group to withstand a herbicide dosage substantially greater than the wild type can withstand (45). Encompassed by the term are preexist­ing lack of susceptibility to herbicides, loss of susceptibility due to selection pressure by a herbicide, and resistance conferred by genetic manipulation, generally in crops. We do not imply in any case that the herbicide induces a

mutation. We know of no data suggesting that mutations resulting in herbicide resistance are caused directly by the herbicide.

RESISTANCE TO AMINO ACID SYNTHESIS INHmITORS

Acetolactate Synthase (ALS) Inhibitors

The chemically dissimilar sulfonylurea, imidazolinone, and triazolopyrimidine herbicide classes share a target site (ALS). Their effIcacy, minimal toxicity to animals, and selectivity in a variety of crops have insured rapid worldwide adoption. ALS inhibitors are selective in crops as diverse as wheat, maize, soybeans, and rice (reviewed in 13, 100).

TARGET SITE ALS (also known as acetohydroxyacid synthase) catalyses the fIrst reaction in isoleucine, leucine, and valine production in a biosynthetic

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HERBICIDE RESISTANCE 205

Table 1 Occurrence and distribution of herbicide-resistant weed biotypes selected under agricul­tural conditions."

Herbicide or class Year first detected Number of species Number of known with resistant biotypes sites

ACCase inhibitors 1982 8 >1000

ALS inhibitors 1986 8 >1000

Amides 1986 2 2

Aminotriazoles 1986 2 2

Arsenicals 1984 1 2

Benzonitriles 1988

Bipyridiliums 1976 18 >50

Carbarnates 1988 2 70

Dinitroanilines 1973 5 >20

Phenoxyacetic acids 1962 6 5

Piclorarn 1988

Pyridazinones 1978 3

Substituted ureas 1983 7 >50

Triazines 1968 57 >1000

Uracils 1988 2 1

'A known site is a site where a resistant biotype is thought to have evolved. Updated from (81, 98) and authors' unpublished data.

pathway found in plants and microbes (reviewed in 163). Bacterial and higher plant ALS is specifically and potently inhibited by sulfonylurea (13, 96, 146), imidazolinone (153), and triazolopyrimidine (166) herbicides in vitro. Inhibition of growth by these herbicides can be reversed by provision of branched chain amino acids (146). Laboratory-generated bacterial (96) and plant (70, 125) mutants possessing herbicide-resistant ALS grow on media containing sulfo­nylurea and imidazolinone herbicides. Similarly, chemically mutagenized Arabidopsis thaliana (70) and Datura innoxia cell cultures ( 149) have produced resistant ALS mutants. Gene transfer technology has provided definitive evi­dence that ALS is the primary target site of these herbicides (70, 181). Resistance in laboratory-generated ALS mutants of maize, tobacco and A. thaliana is conferred by single nuclear genes coding for less-susceptible ALS (26, 70).

RESISTANCE IN CROPS In all crops investigated, resistance to ALS inhibitors is based on enhanced capacity for metabolic inactivation rather than differential rates of herbicide uptake, translocation, or altered susceptibility of the ALS target site (13, 21, 46). Wheat is resistant to chlorsulfuron because of metabolic inactivation involving aryl hydroxylation followed by conjugation to non­herbicidal glucose conjugates (168). Microsomal cytochrome P-450 prepara­tions from maize and wheat catalyze hydroxylation of sulfonylurea herbicides

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206 HOLT ET AL

(49, 185). The same metabolic inactivation pathway can occur in susceptible

species or varieties but with insufficient activity to confer resistance (64). Gene

transfer and tissue culture technology have been exploited to produce transgenic

plants with less-susceptible ALS (113, 125, 127).

RESISTANCE IN WEEDS Many weeds never controlled by ALS-inhibiting her­

bicides are resistant owing to metabolic inactivation (62, 87, 124). Recent

widespread use of sulfonylureas in many crops has resulted in more rapid

selection for weeds resistant to ALS inhibitors than has occurred with other

herbicides. The first weed to exhibit resistance to ALS inhibitors was Lolium

rigidum in Australia, which evolved resistance to the ACCase inhibitor diclofop and exhibited cross-resistance to selective sulfonylureas and imidazolinones

(28,74) (Table 1). Several hundred L. rigidum biotypes have evolved resistance

to diclofop and cross-resistance to ALS inhibitors (136, 137). One mechanism

endowing two of these biotypes with cross-resistance to ALS inhibitors is

enhanced metabolic inactivation (28, 31) rather than a less-susceptible ALS (31,

109). The resistance appears to be a quantitative, polygenic trait.

Resistance in North America has evolved in Lactuca serriola (104), Kochia scoparia (140), Lolium perenne, Salsola iberica (148), and Stellaria media (63). Of greatest significance has been resistance in K. scoparia, with some

500 known resistant sites in North America in 1992 (L. Saari, personal com­

munication). Resistance has also evolved in Sisymbrium orientale and Sonchus oleraceus, although the mechanistic basis of this phenomenon has not

yet been investigated (P. Boutsalis & S. B. Powles, unpublished). Resistance to ALS inhibitors in L. serriola, L. perenne, K. scoparia, S. iberica, S. media,

and in at least one population of L. rigidum (27) is due to mutations to ALS

(38, 63, 148), which is accompanied by different spectra of resistance across a

range of sulfonylureas, imidazolinones, and triazolopyrimidines. A specific

alteration in ALS does not confer automatic cross-resistance across the three

herbicide classes. Given the structural dissimilarity between and within these

classes that share a common ALS binding site (72), it is likely that individual herbicides have overlapping binding niches. Inheritance of ALS resistance in L. serriola is conferred by a single major gene (lOS).

The ALS gene codes for an enzyme of 670 amino acids with a molecular

weight of about 73 kDa-an enzyme highly conserved in various organisms. Mutant ALS genes have been sequenced in a number of plants and microbes

and contain a single nucleotide change resulting in a single amino acid substi­

tution. The DNA sequence change associated with resistance to ALS inhibitors

is a single substitution for proline within one highly conserved region. usually at amino acid 194, in laboratory-generated as well as field-evolved resistance

(70, 99a). The effect of this proline substitution on ALS structure and function

is unknown, although the modified enzyme remains functional.

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HERBICIDE RESISTANCE 207

AGROECOLOGY The appearance of sulfonylurea-resistant weed biotypes within four years of introduction of this herbicide class has raised questions regarding consequences of the resistance mutation and fitness of R biotypes. In greenhouse growth and competition experiments, S L. serriola produced more aboveground biomass and had a higher relative growth rate than R plants in competitive and noncompetitive plantings (1). Competitive ratios of the two biotypes averaged over all treatments were similar, however, indicating that other traits besides shoot growth determine competitive ability in this species. Studies of seed biology showed no differences in fecundity, seed viability, or seed longevity, although R seed germinated faster (2). Given the similar com­petitive ability of S and R L. serriola biotypes,,it is likely that even if sulfonyl­urea herbicides are removed, S biotypes will not replace R ones. Field surveys of the original collection site of R biotypes have confirmed this suggestion. Consequently, management of L. serriola in the field with this herbicide class will be difficult to achieve once the R biotype is present (1).

5-Enolpyruvyl-Shikimate-3-Phosphate Synthase (EPSPS) Inhibitors (Glyphosate)

Glyphosate, the isopropyl amine salt of phosphonic acid, is a post-emergence, nonselective herbicide (reviewed in 43,61). Used in crops and nonagricultural areas for control of most annual and many herbaceous and woody perennial weeds, it has little residual soil activity, is not acutely toxic to mammals, and is toxic to almost all annual plants.

TARGET SITE The primary target of glyphosate is 5-enolpyruvyl-shikimate-3-phosphate synthase, or EPSPS, an enzyme in the shikimic acid pathway that synthesizes aromatic amino acids in plants and bacteria. Shikimic acid accumu­lates after glyphosate treatment, and glyphosate activity can be suppressed by addition of aromatic amino acids (reviewed in 43). Salmonella typhimurium

, with reduced glyphosate susceptibility possess a mutated aroA gene that yields :an EPSPS with decreased affinity for glyphosate (30).

ENGINEERED RESISTANCE IN CROPS Considerable effort has been aimed at development of resistant crop cultivars (reviewed in 17, 45, 113, 127). Glyphos­ate resistance has been engineered into tobacco and tomato by transferring the mutant aroA gene for resistant EPSPS from S. typhimurium (30) and into petunia by introducing genetic constructions from plants for overproduction of EPSPS (127). Resistance to glyphosate has also been enhanced in some species by selection for enhanced EPSPS activity (15).

RESISTANCE IN WEEDS No naturally occurring glyphosate resistance due to resistant EPSPS has been identified. Low levels of resistance are present in some

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208 HOLTET AL

crop and weed species (34), but the physiological basis of this variation is

unknown.

Glutamine Synthetase (GS) Inhibitors

Phosphinothricin (PPT) is a potent new herbicide available as a naturally occurring tripeptide antibiotic, bialaphos, and as a chemically synthesized

herbicide, glufosinate. Bialaphos is produced by fermentation of Streptomyces

hygroscopicus. Glufosinate and bialaphos are nonselective, post-emergence

contact herbicides that are highly effective and rapidly biodegraded.

TARGET SITE PPT is an analog of glutamate that inhibits the amino acid

biosynthetic enzyme glutamine synthase (GS) of plants and bacteria. In plants,

GS is involved in assimilation of ammonia and in regulation of nitrogen

metabolism (reviewed in 97). Inhibition of GS by PPT causes rapid accumula­

tion of ammonia which leads to death of the plant. No naturally occurring

resistance mechanisms are known in plants.

ENGINEERED RESISTANCE IN CROPS Several approaches have been used to engineer plants resistant to GS inhibitors. A PPT-resistant alfalfa cell line with

lO-fold increase in GS activity was used to transform tobacco. Gene amplifica­tion of GS resulted in enhanced GS expression in tobacco, allowing sufficient enzyme activity even in the presence ofthe inhibitors (42, 113, 127). The effects

of this resistance on nitrogen metabolism are unknown. Resistance has also been introduced using the bar gene from S. hygroscopic us, which produces a PPT­detoxifying enzyme. Several transgenic crops produced in this manner are

undergoing field testing (35, 45).

RESISTANCE TO PHOTOSYSTEM II (PSII) INHIDITORS

Triazine, urea, and uracil herbicides inhibit electron transport in photo system II (PSII). Other inhibitors of PSII include bromoxynil and ioxynil,

desmedipham and phenmedipham, propanil, and pyrazon (reviewed in 7). Although structurally diverse, these herbicides or classes inhibit electron trans­

port at a common site (reviewed in 19, 116, 117). Triazines are used for selective pre-emergence and early post-emergence control of annual weeds in crops, primarily com, and for nonselective vegetation control in noncropland. They contain a heterocyclic nitrogen structure that is either symmetrical (s-tri­

azines) or asymmetrical (triazinones). Substituted ureas, including diuron and chlorotoluron, are a large herbicide class produced by substitutions of the hydrogen atoms of urea with other chemical groups, commonly phenyl, methyl, and methoxy. Like triazines, they are relatively persistent in soil, often remaining active for several months.

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HERBICIDE RESISTANCE 209

TARGET SITE The structure and function of PSII and the mechanism of action of PSII inhibitors have been reviewed extensively (19, 95,116, 117, 176). Most electron transport inhibitors bind to the QB site in PSII, thus inhibiting binding of plastoquinone and inhibiting QA oxidation (172). Herbicides and plastoqui­none bind reversibly to overlapping or interacting sites at the acceptor side of PSI!. Biochemical and molecular biological experiments using azidoatrazine, a photoaffinity labeling analog of atrazine, showed that this compound covalently labeled the QB binding protein of PSII (131). The herbicide-binding protein was identified as a 32-kDa protein (also called D l ) that shows a high turnover rate in illuminated leaf tissue (111, 162). The chloroplast gene encoding this protein, the psbA gene, has been sequenced in a large number of algae, cyanobacteria, and higher plants, and is highly conserved (186). Research into the target site of PSII inhibitors has led to an abundance of information about the molecular structure of the PSII reaction center and the D 1 protein (reviewed in 19, 116).

Considerable research has addressed how the many chemicals that inhibit PSII can bind at the same site. PSII inhibitors can be divided into two super­

families, the urea/triazine family and the phenolic family. Within a superfam­ily, compounds of different classes bind to closely overlapping sites, while the

two superfarnilies represent two binding sites that overlap to a lesser extent

(126,173, reviewed in 19).

RESISTANCE IN CROPS s-Triazine herbicides are metabolized in naturally resis­tant crops by several pathways, including 2-hydroxylation, conjugation with glutathione, and to a lesser extent, N-dealkylation of side chains with subsequent oxidation. Com uses all three degradative pathways and is resistant to triazines. Selectivity by substituted ureas is due to limited absorption and translocation, rapid cytochrome P-450 monooxygenase-catalyzed degradation, or oxidation. Thus, most PSII inhibitors are selective by virtue of degradation pathways in crops. Reviews of these mechanisms are found in (7, 68, 69).

Triazine-resistant weeds have been used to generate resistant crops. Resis­

tance has been transferred by sexual crosses from Brassica campestris into

several related cole crops, resulting in release of an atrazine-resistant canola cultivar "Triton" (12). Despite a 20% yield penalty due to R cytoplasm, this cultivar has proved economical in areas where weed densities are high and

triazines are used (50). Efforts to genetically engineer triazine-resistant crops

have been hampered by difficulties in introducing genes into chloroplasts (113). Resistance to metribuzin, due to a single nuclear gene, has been in­

creased in cultivars of tomato and soybean through breeding (45). Resistance to the PSII inhibitor bromoxynil has also been transferred into crops from a bacterium possessing a nitrilase enzyme specific for hydrolysis of bromoxynil (160; reviewed in 127).

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RESISTANCE IN WEEDS R Amaranthus spp., Chenopodium album, and Kochia

scoparia are the most widely distributed and serious triazine-resistant weeds

(98). Triazine resistance is almost always due to a mutation in the chloroplast psbA gene that results in a single serine-to-glycine amino acid change in the D 1 protein of PSII (78). The altered protein has a much lower affinity for triazine

herbicides than the normal protein, resulting in 1 ODD-fold resistance to triazines (6,131). All triazine-resistantpsbA mutants studied have the same serine-to-gly­cine change, although other amino acid mutations in D l have been described for various species of algae and bacteria (reviewed in 19,47, 116). Table 1 shows that among the PSII inhibitors, resistance to the triazines is most pronounced, apparently owing to the specificity that accompanies the serine-to-glycine shift (19). Other mutations confer various relatively low levels of resistance, each to a different spectrum of herbicides, most notably triazines, ureas, and uracils. Because the D 1 protein is a chloroplast gene product, triazine resistance is maternally inherited (159).

A unique case of evolved triazine resistance is found in biotypes of Abuti­Zon theophrasti. Resistance in this weed was shown to be controlled by a single, partially dominant nuclear gene that is not cytoplasmically inherited (4). Unlike most triazine R weed biotypes, R A. theophrasti biotypes are only

10 times as resistant as S biotypes. Resistance in this species is due to en­hanced glutathione S-transferase activity resulting in an enhanced capacity to

detoxify atrazine via glutathione conjugation (5). Chlorotoluron-resistant AZopecurus myosuroides was first detected in En­

gland in 1982 and has now been found at 50 sites (93, 119, 120). Biochemical studies indicate that resistance to chlorotoluron and isoproturon is due to rapid degradation, possibly catalyzed by cytochrome P-450 monooxygenases (92, 93). The mechanism of inheritance is not known, although nuclear inheritance is involved. Biotypes of L. rigidum have recently been found in Australia with

cross-resistance to all PSII inhibitors, including atrazine and chlorotoluron (22). Detoxification by cytochrome P-450 monooxygenases may be responsi­ble for resistance in this biotype as well (22a).

AGROECOLOGY The psbA mutation conferring triazine resistance not only decreases affinity of QB for triazines but also reduces the rate of electron transfer between QA and QB (18, 83, 91). Numerous reports of lower photosynthetic rates, quantum yield, biomass production, fecundity, and competitiveness in R relative to S biotypes confirm the detrimental effect of the resistance mutation (reviewed in 80, 144, 183). The literature is not unequivocal, however; several cases have been reported where R and S biotypes were equally productive (reviewed in 114, 183). Since triazine resistance is maternally inherited, nuclear genome-controlled traits can compensate for detrimental effects of triazine resistance to some extent in field-collected biotypes (114). Recent work with

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HERBICIDE RESISTANCE 211

nuclear-isogenic biotypes has permitted separation of chloroplast and nuclear effects in order to study effects of the triazine resistance mutation alone. Results from these studies have confirmed that impaired chloroplast function in R biotypes limits growth and productivity at the whole-plant level (36, 59, 1 14). Reduced quantum yield, photosynthesis, and growth in high light are due to increased sensitivity to photoinhibition in R plants (65b, 6 6), which limits populations of R plants in the absence of herbicide selection pressure. When plants are grown in low light, differences between biotypes are less pronounced, which may account for persistence of resistance in the field (65b, 66a).

RESISTANCE TO LIPID SYNTHESIS INHIBITORS

Acetyl Coenzyme A Carboxylase (ACCase) Inhibitors

Aryloxyphenoxypropionate (AOPP) and substituted 1,3-cyclohexanedione (CHD) herbicides, although structurally dissimilar, exhibit similar phytotoxic­

ity and symptomology (reviewed in 44, 154). These post-emergence herbi­cides control annual and perennial grass weeds but exhibit little activity against dicots or nongraminaceous monocots. Examples of AOPPs include diclofop and fluazifop; CHDs include sethoxydim and tralkoxydim. Diclofop and tralkoxydim are called selective graminicides because they control grass weeds in the grass crops wheat and barley.

TARGET SITE Plant tissues most affected by AOPPs and CHDs are shoot and root meristems (154). CHDs and carboxylic acids of AOPPs are potent revers­ible inhibitors of plant acetyl-coenzyme A carboxylases (ACCase) (23, 94, 147, 150). ACCases are biotin-containing enzymes found in p1astids, which catalyze ATP- and HC03"-dependent conversion of acetyl-CoA to ma10ny1-CoA. Ma10-ny1-CoA is required for synthesis and elongation of fatty acids and for synthesis of a number of secondary compounds ( 182).

AOPP and CHD graminicides also dissipate transmembrane proton gradi­ents in plant cells (39, 71, 101, 154, 155). It has been suggested that diclofop acts as a proton ionophore or that it binds to a membrane-bound receptor ( 145, 155, 15 6). Although the phenomenon of depolarization is generally accepted, there is disagreement about its role in herbicidal activity (39, 156).

RESISTANCE IN CROPS Dicot and nongrarninaceous monocot crops exhibit intrinsic resistance to AOPP and CHD herbicides. Dicots possess resistant ACCase, and many also exhibit a capacity for detoxification of AOPPs and CHDs. Wheat (Triticum aestivum) and barley (Hordeum vulgare) are resistant only to diclofop and tralkoxydim, while most other major grass crops are susceptible to all registered AOPPs and CHDs. Resistance of wheat to diclofop

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212 HOLT ET AL

and tralkoxydim is due to rapid detoxification (109, 150). Diclofop is demethylated by an extremely active esterase to phytotoxic diclofop acid, then metabolized to nonphytotoxic, water-soluble acidic aryl glycosides by aryl hydroxylation and O-glycosylation (55, 170). Aryl hydroxylation of diclofop acid by wheat microsomes, presumably derived from endoplasmic reticulum, requires 02, is stimulated by light, and is inhibited by l -aminobenzotriazole and other inhibitors of cytochrome P-450 monooxygenases (115, 185). In contrast to wheat, the susceptible grasses maize and oats conjugate diclofop acid to neutral glycosyl esters that remain a potential pool of phytotoxic diclofop acid (154). The rate of glycosyl ester formation in oats can also be slow (84).

Resistance to AOPPs and CHDs has been introduced into crops in labora­tory studies. Resistance to sethoxydim and haloxyfop was selected in maize tissue cultures exposed to sethoxydim (129, 130). In one study resistance was due to increased expression of herbicide-susceptible ACCase (129), while in a second study resistance in regenerated plants was associated with herbicide-re­sistant ACCase (130). Inheritance of the trait was controlled by a partially dominant nuclear mutation. In a subsequent study that identified ACCase mutants with different spectra of herbicide resistance, it was suggested that three, and possibly five, alleles of the maize ACCase structural gene were present (107).

RESISTANCE IN WEEDS A number of weedy grass species are naturally resistant to ACCase-inhibiting graminicides (3, 86). Even in susceptible species such as A vena jatua, variation in herbicide response may be found among local accessions (158). Several grass weeds have evolved resistance to AOPP and CHD herbicides following exposure to these compounds, including Alopecurus

myosuroides in Germany and the United Kingdom (119); Avena sterWs and A.

jatua in Australia and North America (106); Lolium multiflorum in the United

States (161); Lolium rigidum in Australia (72a, 73, 74, 74a), Israel, and the United States; and Setaria viridis in North America (98) (Table 1).

Patterns of resistance to individual ACCase inhibitors in L. rigidum, Avena

spp. and A. myosuroides are not the same for all biotypes. Resistance may be to diclofop only, to all AOPPs but not CHDs, to both herbicide groups, or to CHDs but not AOPPs. Resistance may be present to AOPPs despite exposure only to CHDs, and vice versa. Resistance within a herbicide class or to a single herbicide may also vary considerably (74a, 120).

Herbicide-resistant ACCase has been documented in four grass species (11, 85, 106, 164). In each case the degree of resistance expressed by ACCase reflects the extent of resistance at the whole-plant level. Inheritance of resis­tance in A. sterWs and L. multiflorum is due to a single, partially dominant, nucleus-encoded gene (10, 11, 106). No enhanced herbicide detoxification has been observed (84, 86, 164). It has been suggested that resistance or cross-re-

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sistance to diclofop in A. myosuroides may be due to enhanced activity of a cytochrome P-450-catalyzed detoxification system similar to that in wheat (93). This has yet to be demonstrated unequivocally.

An unknown mechanism of resistance is present in biotypes of L. rigidum

from Australia (71, 84, 155) and a biotype of A. Jatua from Canada (37), which are resistant to AOPPs and cross-resistant to CHDs. This new mechanism is characterized by ability of peeled coleoptile cells or excised roots to regenerate transmembrane electrogenic potentials rapidly following exposure to, and sub­sequent removal of, diclofop acid. These biotypes have susceptible ACCase activities similar to S biotypes and exhibit no increased capacity for detoxifica­tion of diclofop (37, 84, 109).

AGROECOLOGY Little research has been published on effects of AOPP and CHD resistance on fitness of weed biotypes. Recent work with diclofop R and S biotypes of L. multijlorum (B. D. Maxwell, unpublished) and L. rigidum (J. M. Matthews and S. B. Powles, unpublished) demonstrated similar competitive­ness of the two biotypes in monocultures and mixtures. Gene flow studies indicate that pollen dispersal is similar in the two L. multijlorum biotypes; however, S biotypes emerge earlier in the field, have less seed-bank dormancy, and produce seeds earlier relative to R plants (B. D. Maxwell, unpublished). This work indicates that although growth and competitiveness may not be affected by resistance, R and S biotypes may differ in other phenological and phenotypical traits that may be differentially selected by agricultural practices.

RESISTANCE TO AUXIN-TYPE HERBICIDES

Phenoxyacetic Acids

Phenoxyacetic acid herbicides, of which 2,4-D is the most widely used, have as a general structure a phenyl ring attached to an oxygen bonded to an acid. 2,4-D and related herbicides are primarily used for post-emergence dicot weed control in monocot crops, especially maize and wheat.

TARGET SITE Despite 40 years of study, the target site(s) of phenoxyacetic acids have not been established (reviewed in 7, 132). These compounds have growth regulatory effects similar to those of naturally occurring plant auxin hormones. Initially these herbicides cause rapid changes in elasticity of plant cell walls as a result of increased activity of plasma membrane ATPases (29). Symptoms include epinastic bending with subsequent tumor-like unproliferated cell division at growing points, and numerous secondary effects resulting in severe growth abnormalities and uncontrolled cell growth. Although the 2,4-D binding site in plants is unknown, there is speculation that 2,4-D competes with

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auxin hormone for binding to an (unknown) auxin-binding hormone receptor on plasma membranes (29).

RESISTANCE IN CROPS Many monocot crops and weeds are naturally resistant to 2,4-D-type herbicides. Despite long use as cereal-selective dicot-active herbicides, the mechanisms that confer 2,4-D resistance in cereals remain unknown. It is thought that resistance of cereals relative to dicot weeds is due to factors that include differences in rates of herbicide translocation, metabo­lism, and anatomical dissimilarities (reviewed in 132). Wheat can metabolize 2,4-D to nonherbicidal products (20) and it is likely that cytochrome P-450 monooxygenases are responsible for arylhydroxylation of 2,4-D followed by glucosylation. Despite many attempts, only one in vitro study has shown that wheat micro somes can arylhydroxylate 2,4-D (185).

Recent recombinant DNA studies provide definitive evidence that arylhydroxylation by P-450 monooxygenases can confer resistance to 2,4-D and related herbicides. Soil-borne microbial populations, especially Al­

caligenes spp., contain plasmids that confer ability to degrade 2,4-D-type herbicides. A gene coding for a monooxygenase capable of degrading 2,4-D has been identified, cloned, and sequenced from a plasmid of Alcaligenes (41, 165). A single (dominant) gene from Alcaligenes coding for a 2,4-D degrading monooxygenase has been introduced into tobacco, resulting in transgenic plants resistant to high levels of 2,4-D (103, 165). Commercial cultivars of otherwise susceptible cotton plants have recently been transformed with this 2,4-D resistance gene producing transgenic plants resistant to 2,4-D (102). Taken together, these studies establish that increased cytochrome P-450-cata­lyzed metabolism is one mechanism that can confer crop selectivity upon 2,4-D-type herbicides.

RESISTANCE IN WEEDS Despite persistent usage worldwide, 2,4-D and related auxin-type herbicides are remarkably free of herbicide resistance problems. Unequivocal evidence of evolved resistance has been documented in only 6 weeds (Table 1). There have been many reports of differential effects of auxin-type herbicides between biotypes of particular species, but clear evidence of resistance is lacking in most cases (discussed in 8, 58).

In Stellaria media, R and S biotypes have equal rates of herbicide uptake and translocation (33), and despite earlier indications to the contrary (9), there do not appear to be differences in plasma membrane ATPase activity (32). The only observed difference between R and S biotypes is a greater rate of metabo­lism of mecoprop to conjugated metabolites in the R biotype, indicating that increased metabolism (probably cytochrome P-450 monooxygenase-cata­lyzed) may be the basis of resistance (33). Studies with R Sinapis arvensis cannot explain resistance on the basis of differences in rates of herbicide

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uptake, translocation, or metabolism. Given that the mode of action of these herbicides is unknown, it is not surprising that mechanisms conferring resis­tance in S. media and S. arvensis are not established. No studies of genetic control of resistance have been reported.

RESISTANCE TO MITOTIC INHIBITORS

Dinitroanilines

Substituted 2,6-dinitroanilines are selective, soil-active, mainly grass-active herbicides that also control many dicot weeds. Trifluralin, released almost 30 years ago, is the most widely used dinitroaniline. Subsequent introductions were the result of substitutions at ring positions 1, 3, and 4 that alter potency and increase selectivity (reviewed in 141). Dinitroanilines are typically applied preplant or pre-emergence and are incorporated to avoid loss through volatil­ization and photodecomposition. In general, dinitroanilines remain in the

upper layer of soil owing to low water solubility and a tendency to bind organic matter.

TARGET SITE Dinitroaniline herbicides affect cell division, elongation, and differentiation (reviewed in 7, 76). External symptoms include swelling of root tips and inhibition of elongation and lateral root development. Internal symp­toms include formation of large, isodiametric, sometimes polynucleate cells in which mitosis is arrested. Cell walls and plates can be malformed or absent. These symptoms are due to effects of dinitroanilines on tubulin (77). Dinitroanilines bind to plant tubulin heterodimers and inhibit tubulin polymer­ization required for microtubule assembly. Mitosis is arrested at prometaphase, the last mitotic stage not requiring spindle microtubules. Chromosomes con­dense but, owing to lack of microtubules, are unable to move to the poles of the cell. Nuclear membranes reform around the condensed chromosomes resulting in irregular, lobed nuclei.

A suggestion that the effect of dinitroanilines on microtubule formation may be indirect, stemming from effects on intracellular Ca2+ levels (75), has been disputed on the basis that effects on mitochondrial ci+ efflux require herbicide concentrations 100-1000-fold greater than those required to inhibit mitosis (177).

RESISTANCE IN CROPS Dinitroaniline selectivity in crops is enhanced by plac­ing seeds below a herbicide-contaminated soil layer or by delaying planting to allow some degradation of herbicide to occur. Mechanisms responsible for selectivity of dinitroanilines in crops are poorly understood. In general, resis­tance is associated with a low level of herbicide uptake and poor movement

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away from the outermost layers of cells (reviewed in 7, 141). When resistant species grow out of a dinitroaniline-containing soil zone, tissues remaining in the zone often exhibit herbicide-induced symptoms. In some species, resistance may be associated with high levels of lipids into which lipid-soluble dinitroanilines are partitioned.

Although capacities of many plants to metabolize dinitroanilines are poor, some species such as peanuts (Arachis hypogaea), and to a lesser extent soybean (Glycine max), can metabolize at least some dinitroanilines. When metabolism occurs, often trace quantities of numerous degradation products are observed, probably because a number of metabolic pathways are possible. These include N-dealkylation, reduction, oxidation, cyclization, natural prod­uct conjugation, and any combination thereof (reviewed in 141).

RESISTANCE IN WEEDS Dinitroanilines are active on many annual grasses, and to a lesser extent annual dicots, but exhibit poor activity against perennial species. Susceptibility can be associated with small-seededness, lipid-paucity, and having a high proportion of poorly protected meristematic tissue present in the soil-herbicide zone (128, 141). The low incidence of dinitroaniline resistance in weeds may be due to the paucity of detoxification mechanisms in target plants.

Evolved resistance to dinitroaniline herbicides has been reported in Amaranthus palmeri (56) and Eleusine indica (121) in the United States, Setaria viridis in Canada (118), L. rigidum in Australia (74), and A.

myosuroides in England (120) (Table 1). Whereas both highly and moderately resistant biotypes of E. indica are known, S. viridis and L. rigidum biotypes have only moderate resistance.

Mitosis in root tips of highly R E. indica is 1,000-10,000 times as resistant to dinitroanilines and to arninoprophosmethyl (a structurally unrelated herbi­cide) as it is in S plants (178). The R biotype is 50-100 times as susceptible to taxol, a microtubule stabilizing agent, and about 10 times as susceptible to propham and chlorpropham, compounds that cause multipolar mitosis (179). R and S biotypes are equally susceptible to microtubule inhibitors colchicine and DCPA (178). Resistance in S. viridis is moderate (118) and patterns of resis­tance and cross-resistance differ from those of E. indica (157, 177). Mitosis in S. viridis is 2-10 times as resistant to dinitroanilines and arninoprophosmethyl, hypersensitive to chlorpropham but not to taxol, and resistant to DCPA (157). Dinitroaniline resistance in L. rigidum is also moderate to low (74), as is resistance to propham and chlorpropham (F. McAlister, J. A. M. Holtum, and s. B. Powles, unpublished).

Highly R E. indica biotypes contain higher amounts of tubulin and a higher-molecular-weight form of �-tubulin than S biotypes (178, 179). In the presence of oryzalin, equilibrium between free tubulin heterodimers and tubulin polymerized in microtubules may be shifted towards the polymerized

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HERBICIDE RESISTANCE 217

state. It is postulated that in the presence of taxol, microtubules become so stable that normal depolymerization and recycling of free tubulin are retarded sufficiently to inhibit growth. In contrast, S E. indica exposed to 1 �M taxol becomes resistant to trifluralin and oryzalin, despite absence of an altered 13-tubulin. However, taxol-induced resistance in the S biotype does not exactly mimic resistance in the R biotype (179). It has yet to be shown whether hyperstability is due to the presence of altered 13-tubulin or whether the two traits are unrelated.

The mechanism of resistance in moderately R E. indica, S. viridis, and L.

rigidum is unknown but probably differs from that of highly R E. indica.

Moderately R E. indica is not ultrasensitive to taxol nor does it contain an altered tubulin. A variety of resistance mechanisms appear possible. Inheri­tance studies demonstrated that the intermediate form is not a hybrid between Sand R forms (180).

AGROECOLOGY A mutation that confers resistance to dinitroanilines also re­sults in aberrations in some functions of microtubules in the absence of herbicide (179). Growth and development of several R biotypes of E. indica are apparently not impaired by this mutation, although inflorescence dry weight is lower than in S plants (122, 175). R plants are less competitive than S plants and respond to competition by reduced reproductive output (175). These data suggest that dinitroaniline resistance is correlated with reduced fitness. Whether this reduc­tion is due to impaired growth caused by altered tubulin is unknown.

RESISTANCE TO PHOTOSYSTEM I (PSI) INHmrrORS

Bipyridiliums

Two bipyridyl herbicides that primarily affect PSI-paraquat (methyl vio­logen) and diquat-have been in global use for over 30 years. Paraquat and diquat are foliage-active, nonselective herbicides with limited translocation and no soil residual activity because of immediate adsorption to soil colloids (reviewed in 167). Paraquat is more active on monocot and diquat more active on dicot species, although there is substantial overlap. Findings noted here with respect to paraquat apply equally to diquat.

As paraquat is nonselective there are no resistant annual crop species. In the only example of a crop (pasture) species with resistance to paraquat, small differences in paraquat susceptibility between biotypes of Lolium perenne

were exploited in a breeding program to produce a variety of perennial rye­grass that could withstand doses of paraquat lethal to annual weeds (48).

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TARGET SITE To be effective paraquat must enter the chloroplast to reach the site of action at PSI. Within hours (in sunlight) visible damage is evident. Paraquat, a divalent cation, is a PSI electron acceptor that catalytically short-cir­cuits light-driven photosynthetic electron transport by accepting electrons that normally flow to ferredoxin. The paraquat radical reduces oxygen, regenerating paraquat and forming the biologically reactive superoxide radical. While some superoxide is scavenged by superoxide dismutase and related protective en­zymes, excessive superoxide results in production of highly toxic hydroxyl radicals. This toxic form of oxygen reacts with membrane fatty acids (lipid peroxidation) and other cellular components and leads to a rapid loss of membrane integrity, photooxidation, dessication, and plant death (reviewed in 40). Sunlight, by enabling photosynthetic electron transport, greatly effects toxicity of paraquat.

Paraquat is also active in photosynthesizing tissue kept in the dark or in nonphotosynthetic tissue (89, 134). However, symptoms occur more slowly and damage is much less extensive than in sunlight. In such tissue, other electron transport systems probably reduce paraquat, resulting in formation of toxic forms of oxygen, but at a rate much slower than in sunlight.

RESISTANCE IN WEEDS Biotypes of 18 weed species have evolved resistance to paraquat (Table 1). Although there have been mechanistic studies with some R biotypes, there is no clear evidence of resistance mechanisms. These studies have been reviewed recently and therefore are not covered in detail here (40,

53).

There is no evidence that paraquat resistance is due to its restricted uptake into leaf tissue or to altered binding of paraquat within PSI, because photosyn­thetic electron transport is equally affected by paraquat in R and S biotypes (14, 53, 67, 133, 135). Given the rapid action of paraquat in sunlight, it is unlikely that metabolism to a nonherbicidal product could endow resistance. Paraquat has never been shown to be metabolized by plants, either in suscepti­ble species (54), selected R lines of Lolium spp. (67), or evolved R biotypes of Hordeum glaucum or H. leporinum (139).

Resistance to paraquat could be conferred by increased ability to detoxify toxic forms of oxygen produced by electron transfer from the paraquat radical. Plants possess a number of protective enzymes capable of detoxifying toxic oxygen forms and thereby protecting cells from oxidative damage (reviewed in 40,53). Both paraquat R Lolium perenne (65) and Conyza spp. (184) were reported to have increased levels of superoxide dismutase in crude leaf ex­tracts. Isolated chloroplasts from two different populations of R C. bonariensis

had moderately higher activity of superoxide dismutase, ascorbate peroxidase, and glutathione reductase (108, 152). However, studies with R C. canadensis

(133), C. philadelphicus (169), Ceratopteris richardii (24) and H. glaucum

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HERBICIDE RESISTANCE 219

(135) show no increase in activity of oxygen protective enzymes. There is evidence with R biotypes of C. canadensis (53, 169), C. philadelphicus (169), and H. glaucum (14) that paraquat mobility is retarded in R but not S plants. Recent studies with R H. glaucum and H. leporinum confirm that little para­quat reaches meristems to disrupt PS I (139). Although it is clear that one paraquat resistance mechanism involves restricted mobility of paraquat, nei­ther the molecular mechanism restricting mobility nor the site(s) of compart­mentation have been identified. A polyamine transport system may be in­volved in uptake of paraquat into cells of S plants (65a). Resistance in C.

bonariensis (151), C. philadelphicus (90), and H. glaucum (88) was conferred by a single dominant nuclear gene.

AGROECOLOGY ParaquatR C. canadensis was less vigorous than the S biotype in the absence of paraquat (89). Field studies with Rand S H. glaucum, H. leporinum, and Arctotheca calendula in Australia demonstrated a slight reduc­tion in competitiveness of R H. glaucum relative to S plants (174) whereas R and S H. leporinum were equally competitive (E. Purba, C. Preston, and S. B. Powles, unpublished). Seeds of R and S H. glaucum germinated equally well after ripening, and in the absence of fresh seed production, seed-bank reserves were depleted within three years. These results show that populations of the R biotype can be significantly reduced by prevention of seed production for three successive years (138). In contrast, seed-bank longevity inA. calendula is much greater, such that even after six years of prevention of seed production, viable R seeds remain in the soil (T. W. Morgan, E. S. Tucker, S. B. Powles, unpublished).

CROSS- AND MULTIPLE-HERBICIDE RESISTANCE

The terms cross- and multiple-resistance are often used interchangeably. Mul­tiple-resistance is the phenomenon of resistance to herbicides from more than one chemical class to which a population has been exposed. Cross-resistance is the phenomenon whereby, following exposure to a herbicide, a weed popula­tion evolves resistance to herbicides from chemical classes to which it has never been exposed. Because both multiple- and cross-resistance can occur in a single population (74a, 120), identification of the phenomenon requires accurate records of herbicide exposure. Multiple-resistance, although uncom­mon, is increasing in frequency as weed populations are exposed to a greater diversity of herbicide chemistries. Examples of multiple-resistance include C.

canadensis that had been exposed to, and evolved resistance to, PS I- and PS I I-inhibiting herbicides (133); resistance to triazines and substituted ureas in

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A. myosuroides (120); and repeated evolution of resistance to AOPP and

ALS-inhibitors in L. rigidum (72a).

The commonest form of cross-resistance occurs when different herbicide

chemistries act on the same target site; thus an alteration in the target that gives

resistance to one herbicide class may also give resistance to the unseen herbi­

cide class. In weeds resistant to AOPPs due to herbicide-resistant ACCase,

resistance is often, but not always, accompanied by cross-resistance to some

CHD graminicides (85, 107, 129). Similar observations have been made with

ALS inhibitors (72), PSII inhibitors (52), and mitotic inhibitors (178). Often resistance across chemical classes is not complete, usually because binding

sites of the chemical groups are not homologous. For example, although both

triazine and substituted urea herbicides inhibit PSII by binding to the same

32-kDa protein, no cases are known in higher plants where triazine resistance resulting from an alteration in the binding protein has conferred cross-resis­

tance at the whole-plant level to substituted ureas (113).

Cross-resistance that is not due to different chemistries' having similar

target sites is rare in plants but has been described repeatedly for insects (19a). The best-documented examples of cross-resistance in plants are for L. rigidum

and A. myosuroides, both annual grass weeds that have been exposed to a range of herbicides since the mid-1970s. Following exposure to the triazine

atrazine and the triazole amitrole for 10 years, a L. rigidum biotype evolved multiple-resistance to triazines and amitrole and exhibited cross-resistance to all PSII inhibitors (22). Cross-resistance to substituted ureas was due not to

changes in the D 1 PSII protein but to an increased ability for oxidative metab­olism (22a). Metabolism is probably responsible for cross-resistance in some

A. myosuroides populations (93) in which the chief selection pressures were the substituted ureas chlorotoluron and isoproturon and the AOPP diclofop.

Patterns of resistance within herbicide classes-for example, resistance to

dic1ofop but not fluazifop (AOPPs), pendimethalin but not trifluralin

(dinitroanilines), and tralkoxydim but not sethoxydim (CHDs)-are consistent

with ease of oxidative metabolism, probably by cytochrome P-450 monooxygenases (93).

Several hundred biotypes of L. rigidum have evolved cross-resistance to wheat-selective ALS inhibitors following exposure to the mitotic-inhibitor

trifluralin and the ACCase-inhibitor diclofop (73, 74, 85). The simplest expla­

nation is that a mechanism that gives resistance to either trifluralin or diclofop must give cross-resistance to ALS inhibitors. However, sulfonylurea resis­

tance is associated with increased oxidative metabolism (28, 31), whereas the

mechanism of dic1ofop resistance in weeds, although unknown, is not in­creased metabolism (71, 84, 109). It has yet to be established whether triflura­lin resistance results from increased metabolism.

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AGROECOLOGY L. rigidum R biotype SLR 31 has been shown in field compe­tition experiments to perform as well as the S biotype, suggesting that possession

of several mechanisms of resistance does not necessarily reduce vigor. This species also has relatively short seed-bank longevity, which facilitates weed

control when seed production is prevented (J. M. Matthews, S. B. Powles,

unpublished).

AGRONOMIC IMPLICATIONS OF HERBICIDE RESISTANCE

Although herbicide resistance is a worldwide phenomenon, traditionally there

has been little need for development of special control strategies for resistant

biotypes because control has usually been accomplished with alternative her­

bicides. Over the last 10 years, however, resistance in weeds has increased at a

rate equivalent to that of insecticide and fungicide resistance (82). As a result,

crop and weed management practices, especially choice and combination of

herbicides, have been changed in some locations. In addition, multiply-resis­

tant weed populations cannot be managed simply by changing herbicides,

since any new herbicide that is used persistently has a high probability of

selecting for resistance and thus becoming ineffective (137). In addition, herbi­

cide rotations or mixtures may not delay the rate of appearance of resistance in

cases where fitness of R biotypes is nearly the same as that of S biotypes.

Effective management of herbicide resistance in weeds depends on reduc­

ing selection pressure for evolution of resistance (58, 60, 112), which of

necessity involves reducing the frequency and amount of herbicide applied

and increasing reliance on integrated management practices. Models of dy­

namics of resistant and susceptible weed populations are becoming useful for

understanding factors that determine rates of evolution of resistance in the

field, particularly fitness and gene flow, and for designing appropriate man­

agement strategies (60, 112, 142). Potential introductions of herbicide-resis­

tant crops will add complexity to resistance management, particularly in cases

where escape of engineered genes is likely (45, 79). While certain benefits

may be realized from using herbicide-resistant crops, resistant-weed problems

may be exacerbated when appropriate resistance management is not practiced.

Regardless of whether resistance has appeared in a field, crop production

systems that involve use of herbicides should always incorporate practices to

prevent and manage for its eventual occurrence. Biochemical and agroecologi­

cal research is needed in order to develop a better understanding of the causes

and consequences of herbicide resistance in weeds and crops.

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