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Herbicide Cross Resistance and Multiple Resistance in Plants
Stephen B. Powles and Christopher Preston
Department of Crop Protection, Waite Agricultural Research Institute, University of Adelaide, South Australia, 5064

Table of Contents
I. Introduction
II. Part A. Cross Resistance to Herbicides
1)

Section 1: Target Site Cross Resistancea. Resistance to ALS-inhibiting
herbicides
b. Resistance to ACCase-inhibiting
herbicides
c. Resistance to PS2-inhibiting
herbicides
d. Resistance to other modes of action

2)

Section 2: Non Target Site Cross
Resistancea. Resistance to ALS-inhibiting
herbicides
b. Resistance to ACCase-inhibiting
herbicides
c. Resistance PS2-inhibiting herbicides

III. Part B. Multiple Resistance to Herbicides
IV. Conclusions and Future Directions
V. References

I. Introduction
It is now well established that persistent herbicide
application to a plant population is a strong selection
pressure for individuals carrying genes conferringherbicide resistance. Plants expressing any
genetically-endowed traits enabling survival in thepresence of the herbicide have a strong advantage
and may come to dominate the population.
The severity and time period over which resistancecan develop varies dependent upon the herbicide(s)used and biological, agro-ecological, and managerial
factors, but can be as short as three years fromcommencement of herbicide use (Tardif and Powles,
1993). For an overview of the herbicide resistanceliterature, the reader is referred to the published book	
  proceedings from a number of international meetings(LeBaron and Gressel, 1982; Green et al., 1990;
Caseley et al., 1991; Denholm et al., 1992), as well asa very recent book (Powles and Holtum, 1994).
This contribution does not seek to review herbicide
resistance in general, but rather to concentrate on the
more recent phenomena of herbicide cross resistanceand multiple resistance.

II. Part A. Cross Resistance to Herbicides
Cross resistance is defined as the expression of agenetically-endowed mechanism conferring the ability
to withstand herbicides from different chemicalclasses. Following Hall et al. (1994), we have chosen
to use mechanism-based definitions for crossresistance as these have the advantage overherbicide history definitions in that herbicide histories
may be incomplete, and do not allow for the
introduction of resistance genes via seed or pollen.
There is a disadvantage in that the mechanism(s) ofresistance to herbicides must be known before an
assignment can be made.
There are two broad cross resistance categories;
target site cross resistance (considered in Section 1)
and non target site cross resistance (considered in
Section 2). The phenomenon of cross resistance isimportant from both a practical and scientificviewpoint. Agricultural producers and/or agrochemical
manufacturers can experience substantial economic
loss and other problems if cross resistance to a rangeof herbicides limits weed control options. Unravellingthe biochemical and genetic basis of cross resistance,
as well as implementing sustainable weed control
programs, are important scientific challenges.
This review considers many examples of herbicideresistant populations of the grass species Lolium
rigidum and Alopecurus myosuroides because these
species are the first to display widespread herbicide
resistance across a range of chemical classes (seeHall et al., 1994). L. rigidum is an annual, diploidcross-pollinated species native to the Mediterranean
and now widely dispersed in some regions of theworld with a Mediterranean-type climate. L. rigidum isa widespread, abundant weed within the cropping
regions of southern Australia where it decimates crop
yield if not controlled. Herbicides have been widely
employed to control L. rigidum and within a few yearsof use, herbicide-resistant biotypes became evident.
Since the first report in 1982 (Heap and Knight, 1982),
the occurrence of resistance has dramaticallyincreased. What is striking about herbicide resistance	
  in L. rigidum in Australia is the complex resistancepatterns which develop across many different
herbicide groups. In some populations resistanceexists to just one herbicide group, whereas in otherpopulations resistance extends across many
herbicide groups and modes of action. Resistance tomany herbicides makes L. rigidum control in Australia
a significant practical problem (Powles and Matthews,
1992).
A. myosuroides is also an annual, diploid, crosspollinated species with high fecundity and is a major
weed in parts of Northern Europe. Resistance totriazine herbicides in A. myosuroides was reported in
Israel in 1982 (Yaacoby et al., 1986). Concurrently, or
soon thereafter, populations resistant to substituted
urea herbicides were reported in Germany (Niemann
and Pestemer, 1984) and the U.K. (Moss andCussans, 1985). Cross resistance has been
documented in biotypes in England (Moss, 1992) andSpain (De Prado et al., 1991). In common with L.
rigidum, many biotypes of A. myosuroides exhibit
cross resistance to herbicides from a variety ofherbicide classes (Moss, 1990; De Prado et al.,1991). However, the areas infested are not large andthe number and severity of resistant populations are
only a fraction of the resistant L. rigidum populations
in Australia. Both A. myosuroides and L. rigidum
exhibit many characteristics that favor theaccumulation of herbicide resistance mechanisms.
These characteristics include large populations ofwidespread distribution in cropping areas, highreproductive capacity, rapid seed bank turnover,allogamous reproduction, and genetic and phenotypic
plasticity (Moss and Cussans, 1985, Powles andMatthews, 1992).
Numerous herbicide-resistant biotypes of both L.
rigidum and A. myosuroides have been documented.
Amongst these there are a wide range of resistanttypes and resistance patterns. Several biotypes ofboth species will be considered here, and to avoid
confusion, the original published biotype names havebeen retained. These are listed in Tables 1 and 2
for L. rigidum and A. myosuroides, respectively, andgive the resistance spectrum and types of resistancemechanisms, where known, for each biotype. The
herbicide histories (not provided) of these biotypes
range from simple to extremely varied. Salientfeatures of the herbicide histories of these biotypes
will be provided in the text.

1) Section 1: Target Site Cross ResistanceTarget site cross resistance occurs when a change atthe biochemical site of action of one herbicide also
confers resistance to herbicides from a different
chemical class that inhibit the same site of action in
the plant. Target site cross resistance does notnecessarily result in resistance to all herbicide classes
with a similar mode of action or indeed all herbicides

within a given herbicide class. While there are many
examples of target site cross resistance, some of themost important examples are summarized below:
a. Target site cross resistance to acetolactate
synthase (ALS)-inhibiting herbicides
Over the past decade, the most important area of
herbicide chemistry has been the discovery ofherbicides inhibiting acetolactate synthase (ALS).
There are 15 classes of chemistry which have been
described as inhibitors of ALS (Saari et al., 1994).
Of these, the chemically dissimilar sulfonylurea,
imidazolinone and triazolopyrimidine herbicides havebeen commercialized and are in widespread use.
The large scale adoption and often persistent use of
these herbicides has led to the appearance of weed
biotypes resistant to the ALS-inhibiting herbicides.
As reviewed by Saari et al. (1994), there are now
many biotypes within at least 15 weed species(especially Kochia scoparia and Lolium rigidum)
which have developed resistance to ALS-inhibiting
herbicides, mainly through selection with sulfonylurea
herbicides (presumably because they have been incommercial use for the longest period). In the vast
majority of cases of resistance following selection withsulfonylurea herbicides, the resistance mechanism isa change in the target site enzyme ALS (reviewed by
Saari et al., 1994). In most cases, the sulfonylurearesistant biotypes with a resistant ALS enzyme exhibit
varying levels of target site cross resistance to thechemically dissimilar, but ALS-inhibiting,imidazolinone and/or triazolopyrimidine herbicides(Table 3; Hall and Devine, 1990; Christopher et al.,
1992; Saari et al., 1990; 1992; 1994).
The considerable variation in the level of resistanceacross and within various ALS-inhibiting herbicide
chemistries (Table 3) is likely to be due to subtly
different binding by particular herbicides on the ALS
enzyme and different mutations of ALS. Evidence
from competitive binding studies show that the threeclasses of ALS-inhibiting herbicides bind to the same,or closely overlapping sites on ALS (Durner et al.,
1991; Landstein et al., 1993). The wide variation intarget site cross resistance amongst biotypes withresistant ALS enzyme (Table 3) implies that there are
a number of different functional mutations of the ALS
gene. Knowledge of specific mutations of ALS
providing resistance is now emerging. ALS genesequences from a number of resistant biotypes ofhigher plants which have been examined show asubstitution at a proline residue (173) in a highly
conserved region of the enzyme, known as domain A.
However, the proline substitutions vary in that
substitutions of threonine, alanine, serine, histidine
and glutamine for this proline have all been observed.
Guttieri et al. (1992) examined ALS from threeresistant weed species and observed Thr substitution
in Kochia scoparia and a His substitution in Lactuca
serriola at Pro 173. No alteration was observed in

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domain A of ALS for a resistant biotype of Salsola
iberica. Five other resistant biotypes of K. scoparia
were examined and only three contained asubstitution at Pro 173. In addition to changes at the
Pro 173 of domain A, at least two other mutations
have been observed to give sulfonylurea and/or
imidazolinone resistance in higher plants; Ser 653
Asn in Arabidopsis thaliana (Sathasivan et al., 1991),
and Trp 573 Leu in Nicotiana tabacum (Lee et al.,1988), and a number of other mutations providing
resistance are known from yeast (Mazur and Falco,1989). Significantly, in the only case so far publishedof resistance selected by an imidazolinone herbicide,a biotype of Xanthium strumarium resistant toimidazolinone herbicides at the whole plant and ALS
enzyme level is not cross resistant to sulfonylurea or
triazolopyrimidine herbicides and possesses an ALS
enzyme susceptible to these herbicides (Schmitzer etal., 1993). Therefore, it is clear that there are several
possible mutations of the ALS gene which will confer
resistance to sulfonylurea and imidazolinone
herbicides and yet retain enzyme function. It is likely,
although not yet established, that these different
mutations in the ALS gene provide different levels oftarget site cross resistance within and between ALSinhibiting herbicide chemistries. The variations intarget site cross resistance among herbicide-resistantmutants indicates that the binding domains for thevarious classes of ALS-inhibiting herbicides do not
fully overlap. It is also clear from these studies that a
number of different mutations can endow resistanceto various ALS-inhibiting herbicides without any
significant impairment of enzyme function in vivo. As
discussed below, this is also likely to be the case forherbicide-resistant ACCase, but is not the case forherbicide-resistant PS2 in which very few mutations
confer resistance and yet retain full enzyme
functionality. Competitive fitness studies with ALS
enzyme-based resistant biotypes of Kochia
scoparia and Lactuca serriola indicate there is no
fitness penalty to plants carrying a resistant ALS
enzyme (Mallory-Smith et al., 1992).
b. Target site cross resistance to acetyl-CoA
carboxylase (ACCase)-inhibiting herbicides
During the 1970s and 1980s, two chemicallydissimilar herbicide groups, thearyloxyphenoxypropionic acid (APP) andcyclohexanedione (CHD) herbicides, which target theplastid enzyme ACCase, were commerciallydeveloped and widely adopted. These herbicides arelethal to many Graminaceae but are harmless to dicot
species and have therefore become widely employed
for grass weed control. Following widespread usageof ACCase-inhibiting herbicides, resistance to thesemodern generation graminicides has become
extensive in L. rigidum in Australia and is developing
rapidly in the closely related L. multiflorum in Oregon,
in wild oats (Avena spp.) in Australia and N. America,
and in other species (for a review of resistance to

ACCase herbicides see Devine and Shimabukuro,1994).
In L. rigidum in Australia, and L. multiflorum in North
America, many ACCase target site-based resistantbiotypes have appeared (Stanger and Appleby, 1989;
Holtum and Powles, 1991; Gronwald et al., 1992;
Tardif and Powles, 1993). In L. rigidum, selection
either with an APP herbicide (Holtum and Powles,
1991), or a CHD herbicide (Tardif et al., 1993), has
led to target site cross resistance to both the APP and
CHD herbicides, however in both cases, the level ofresistance to APPs is greater than that to CHDs
(Table 4). It is evident from the data collated in Table
4 that different resistant L. rigidum biotypes
possessing resistant ACCase exhibit different
patterns of resistance at the whole plant level and in
ACCase assays (Tardif and Powles, 1993). Many, but
not all, L. rigidum biotypes exhibit target site crossresistance across the APP and CHD herbicide
chemistries. In contrast, a biotype of L. multiflorum
selected with diclofop-methyl and with an ACCase
resistant to APP herbicides shows no target site crossresistance to the CHD herbicides (Gronwald et al.,1992). Two biotypes of A. myosuroides (Mason andOtmoor) have been documented as highly resistant to
the APP herbicides as a result of resistant ACCase(Hall, Moss and Powles, unpublished). The ACCase
from these biotypes is also resistant to CHD
herbicides. Resistance to APP herbicides in several
biotypes of the wild oat species Avena fatua andAvena sterilis is also endowed by resistant forms of
the ACCase enzyme. In these cases, there are
varying degrees of target site cross resistance to the
CHD herbicides, ranging from none to moderate(Maneechote et al., 1994; Maneechote, Preston andPowles, unpublished). These levels of target site
cross resistance to the CHD herbicides at the wholeplant level correlate with the level of resistancedisplayed by ACCase from these biotypes(Maneechote, Preston and Powles, unpublished).
From the foregoing it is clear that target site-based
resistance to ACCase herbicides does not always
lead to cross resistance to other herbicides with thesame site of action. This is the expected result where
herbicides from different chemical classes bind tooverlapping, but not identical sites on the target
enzyme (see also (a) above and (c) below). This is
likely, although not yet established at the molecularlevel, for APP and CHD herbicides interacting with
ACCase. The patterns of resistance of ACCase toherbicides can be strikingly different even among
resistant biotypes of the same species as can beseen from Table 4. For example, among biotypesof L. rigidum, resistance to haloxyfop can range frommoderate to high, and resistance to sethoxydim canrange from nonexistent to moderate. Therefore, wesuggest the differences in target site cross resistanceare the result of selection for different mutations of the
ACCase gene in different resistant populations.

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Evidence exists from maize cell lines that different
alleles at the same locus encode different resistantforms of ACCase with different levels of target site
cross resistance (Marshall et al., 1992). Thereremains a wealth of valuable information to beobtained from these various ACCase mutants. While
the ACCase gene has recently been sequenced froma number of plant species (Roessler and Ohlrogge,
1993; Ashton et al., 1994; Ellborough et al., 1994;
Shorrosh et al., 1994) there is, as yet, no specificknowledge of herbicide binding site(s) within the
ACCase enzyme. The various different herbicide
resistant ACCase mutants (Table 4) will be very
useful in elucidating herbicide binding and the specificmutations which endow resistance while retaining
enzyme functionality.
A second site of action has been proposed for APP
and CHD herbicides. These herbicides cause a rapid
depolarization of plant cell membrane potentials by
allowing the influx of protons (Lucas et al., 1984;
Shimabukuro, 1990). The maintenance of anelectrogenic potential is vital to survival of the cells,
however, the importance of the herbicide-induced
depolarization of the membrane potential as aherbicidal mode of action has been questioned(DiTomaso et al., 1991). Also, the relevance of theherbicide-induced depolarization of the membranepotential to the field performance of these herbicides
is entirely unknown. Cells from root tips andcoleoptiles of some biotypes of L. rigidum resistant to
APP and CHD herbicides are able to re-establish themembrane potential following removal of herbicidefrom the bathing solution (Häusler et al., 1991; Holtum
et al., 1991; Shimabukuro and Hoffer, 1992). Thisability to repolarize the membrane potential following
removal of the herbicide is not observed withsusceptible biotypes. Similar results have beenobtained with a herbicide-resistant biotype of Avena
fatua (Devine et al., 1993), however, in other resistantbiotypes of A. fatua and A. sterilis repolarization of themembrane potential does not occur following removalof the herbicide (Maneechote et al., 1994;
Maneechote, Preston and Powles, unpublished).
Repolarization of the membrane potential occurred inresistant L. rigidum biotypes irrespective of thepossession or absence of a resistant ACCase.
Repolarization is pH dependent even in susceptible
biotypes (DiTomaso, 1993; Holtum et al., 1994;
Maneechote, Preston and Powles, unpublished). The
biotypes of L. rigidum which show repolarization of
the membrane potential following removal of theherbicide also displayed a reduced ability to acidify
the external solution bathing roots or coleoptiles(Häusler et al., 1991; DiTomaso, 1993). DiTomaso(1993) claimed a direct connection between the
differential abilities of the resistant L. rigidum biotypes
to acidify the external medium and the repolarizationof the membrane potential following removal of theherbicide. In contrast to the above, the biotype of
A. fatua displaying the membrane repolarization

phenomenon acidifies the external medium at thesame rate as the susceptible biotype (Devine et al.,1993). There is still a myriad of unsolved questions
regarding the repolarization of the membranepotential and its role, if any, in resistance to APP and
CHD herbicides (see Holtum et al., 1994). What isclear is that there may be a fundamental difference inmembrane properties of some resistant biotypes of
L. rigidum compared to the susceptible biotypes(Häusler et al., 1991). What relevance this has toherbicide resistance is unclear.
c. Target site cross resistance to photosystemtwo (PS2)-inhibiting herbicides
Numerous chemically dissimilar herbicide classes act
by inhibiting photosynthetic electron transfer at
photosystem two (PS2). The extensively studied andwidely used triazine and substituted urea herbicidegroups are toxic to plants because they are potent
and specific inhibitors of photosynthesis at PS2.
These herbicides bind to the QB binding site on the
D1 protein within the PS2 reaction center. Triazine
herbicides have been persistently used for weed
control in maize production in many parts of the world
and this practice has led to widespread resistance intarget weeds. The first report of herbicide resistanceinvolved a triazine herbicide (Ryan, 1970), and sincethen triazine resistance has become the mostprevalent and well characterized example of herbicide
resistance world-wide, with resistance documented inbiotypes of more than 60 species (LeBaron, 1991).
For a review of resistance to PS2 herbicides see
Gronwald (1994). With a few exceptions, triazine
resistance is due to target site resistance endowed bya modification at the herbicide target site, the D1
protein of PS2 (reviewed by Gronwald, 1994).
It is noteworthy that biotypes highly resistant totriazine herbicides as a result of a modified D1 protein
are not resistant to the chemically distinct substituted
urea herbicides (Table 5), despite the fact that thesubstituted urea herbicides are also potent PS2
inhibitors (reviewed by Gronwald, 1994). The
substituted urea and triazine herbicides bind tooverlapping, but not identical, sites in PS2 (reviewed
by Trebst, 1991). As a result, the mutation Ser 264
Gly providing resistance to triazine herbicides does
not affect binding of substituted urea herbicides(Arntzen et al., 1982; Trebst, 1991). In contrast, asshown in Table 5, plants containing triazine-resistantPS2 are resistant to other PS2-inhibiting herbicide
chemistries including the triazinones, uracils, andpyridazinones (Fuerst et al., 1986; Ducruet and De
Prado, 1982; Oettmeier et al., 1982; De Prado et al.,1989). It is somewhat surprising that there are varying
degrees of target site cross resistance to other PS2
inhibitors between species (Table 5), as all known
triazine-resistant PS2 from higher plants contain thesame Ser 264 to Gly substitution in the D1 protein(Trebst, 1991). The explanation for this variation

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probably lies in the use of isolated thylakoids versus
intact chloroplasts for measuring target site
resistance, as the chloroplast envelope probably
provides a differential barrier to these herbicides.
Additionally, differences between species in the
structure of the reaction center proteins surrounding
the active site might contribute to greater or lesser
sensitivity of the active site to different classes ofherbicide.
A range of mutations within the QB binding site of theD1 protein providing resistance to triazine herbicides
have been identified in unicellular algae suchas Chlamydomonas, Euglena, Synechocystis,and Synechococcus (Trebst, 1991). Despite thesevarying mutations in lower plants, in higher plants only
one mutation (Ser 264 Gly) has been identified intriazine-resistant weed species (Trebst, 1991). Thismutation leads to a reduction in the capacity forphotosynthetic electron transport between QA and QB(Bowes et al., 1980; Ort et al., 1983), which in turnleads to an increased susceptibility to photoinhibitionin the resistant biotypes (Hart and Stemler, 1990a;
Sundby et al., 1993). Such triazine-resistantindividuals display a marked decrease in growth rate
at normal light intensities (Hart and Stemler, 1990b)
and a reduction in competitive fitness (reviewed in
Holt and Thill, 1994). It appears likely that the othermutations within the QB binding site are even moredetrimental to fitness and therefore, have notpersisted in the wild.
It is therefore clear that for triazine resistance inhigher plants a single mutation of Ser 264 Gly within
the QB binding site on the D1 protein confers
resistance, with no other target site mutations yet
identified. Evidently, only this specific mutation canendow resistance while retaining enzyme
functionality, despite selection of countless numbersof plants with triazine herbicides in many parts of theworld. However, it is not wise to generalize from PS2
target site resistance to that which might occur withanother herbicide target site enzyme. As discussed in(a) and (b) above, a different situation prevails fortarget site ALS or ACCase herbicide resistance inwhich there are likely to be several mutations which
endow resistance while retaining enzyme
functionality. In reality, for a particular enzyme
targeted by herbicides, there could be from zerothrough to several potential mutations of the target
enzyme which could endow herbicide resistance while
retaining enzyme functionality. It is only after billionsof plants have been exposed to herbicides acrossvast areas that the full array of potential for functional
mutation of a herbicide target site becomes apparent.
Following such widespread selection both ACCaseand ALS exhibit several different mutations which
endow herbicide resistance, whereas only one
mutation has appeared in the D1 protein of PS2.
Clearly, a variety of mutations providing resistancecan be readily accommodated in some herbicide

target sites while retaining enzyme functionality but
few or no mutations providing resistance can beaccommodated by other herbicide target sites.
d. Resistance to other modes of action
There have been few reports of target site resistanceto herbicides with modes of action other than ALS,
ACCase, or PS2. Where such reports are available,
there are few cross resistance studies and relatively
few studies with the target site in vitro. Two cases
where target site cross resistance is evident arebriefly described below:i.

Selection by dinitroanilines for biotypes
of Eleusine indica which are resistant todinitroaniline herbicides as a result of aherbicide-resistant microtubule assembly,
are also resistant to amiprophosmethyl, amicrotubule disrupting herbicide from adifferent chemical class (Vaughn et al.,
1987; Vaughn and Vaughan, 1990). The
exact basis of resistance in this biotype
has not been established (Smeda andVaughn, 1994).

ii.

A biotype of Sinapis arvensis is resistantto a wide range of auxinic herbicides
including dicamba, MCPA, mecoprop,
2,4-D, and picloram. The mechanism of
resistance to these herbicides in thispopulation has not been firmly
established, but is probably the result of amodification of the auxin receptors(Peniuk et al., 1993).

2) Section 2: Non Target Site Cross
ResistanceNon target site cross resistance is defined as crossresistance to dissimilar herbicide classes conferred bya mechanism(s) other than resistant enzyme target
sites. Until recently documented for L. rigidum andA. myosuroides, non target site cross resistance waslargely unknown in herbicide-resistant weeds but iswell known in the insecticide resistance literature(Brattsten et al., 1986; Georghiou, 1986).
The evidence for non target site cross resistance inL. rigidum and A. myosuroides is presented below.
a. Non target site cross resistance to ALSinhibiting herbicides
The study of Heap and Knight (1986) and widespread
farmer experience in Australia has been that many(but not all) L. rigidum populations that developed

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resistance following selection with the ACCaseinhibiting herbicide diclofop-methyl display resistanceto cereal-selective ALS herbicides without any
exposure to ALS herbicides (non target site crossresistance). Similarly, a laboratory experiment
Matthews and Powles (unpublished data) showed thatan initially susceptible L. rigidum population whenselected for three generations with diclofop-methyl
developed resistance to diclofop-methyl andsimultaneously exhibited resistance to the ALSinhibiting herbicide chlorsulfuron without any
exposure to chlorsulfuron. This study and the fieldobservations conclusively established that selection
with an ACCase-inhibiting herbicide can lead toresistant populations that display non target site crossresistance to ALS-inhibiting herbicides without
exposure to these herbicides.
The mechanistic basis of non target site crossresistance to ALS herbicides has been thoroughly
investigated in L. rigidum. As expected, crossresistance to ALS herbicides from selection with
ACCase herbicides is not due to resistance at the
ALS target enzyme (Matthews et al., 1990). Insteadthese biotypes of L. rigidum are resistant as a resultof an enhanced rate of herbicide metabolism, which
endows resistance to certain ALS-inhibiting herbicides(Figures 1 and 2). It is likely that the increased
metabolism in these L. rigidum biotypes is catalyzed
by the same Cyt P450 enzyme-based mechanism
operating in wheat (Christopher et al., 1991; 1992).
Wheat is resistant to many ALS-inhibiting herbicides
as a result of rapid metabolism of these herbicides byaryl-hydroxylation (Sweetser et al., 1992), catalyzed
by a Cyt P450 mono-oxygenase. Some chlorsulfuronresistant L. rigidum biotypes with sensitive ALS and a
resistance profile to ALS-inhibiting herbicides similar
to wheat can oxidatively metabolize chlorsulfuron
more rapidly than the susceptible biotype (Figures 1
and 2; Christopher et al., 1991; Cotterman and Saari,
1992; Burnet et al., 1994a). The products ofmetabolism of chlorsulfuron in L. rigidum and wheat
are also similar (Christopher et al., 1991; Cotterman
and Saari, 1992), with the major metabolite identified
as glucose-conjugated hydroxy-chlorsulfuron(Cotterman and Saari, 1992). Malathion which has
been shown to inhibit the Cyt P450-dependent
detoxification of primisulfuron, a sulfonylurea
herbicide, in microsome preparations from maize(Kreuz and Fonné-Pfister, 1992) can inhibit
chlorsulfuron metabolism and reduce chlorsulfuron
resistance in the cross-resistant biotype SLR31 if
applied in conjunction with chlorsulfuron (Christopher
et al., 1994). This reversal of resistance in SLR31 bymalathion confirms that detoxification plays a majorrole in chlorsulfuron resistance in this biotype.
Taken together, these studies clearly establish thatenhanced metabolism is the basis of non target site
cross resistance of L. rigidum to ALS herbicides. Cyt
P450s are clearly implicated in enhanced metabolismof chlorsulfuron in resistant L. rigidum, however, the invitro demonstration of Cyt P450-dependentchlorsulfuron metabolism in isolated microsomes has
to date proved elusive (Preston and Powles,
unpublished).
b. Non target site cross resistance to ACCaseinhibiting herbicides
Over the past decade in Australia, the ACCaseinhibiting herbicide diclofop-methyl has been annuallyapplied to millions of hectares of cereal crop tocontrol L. rigidum and wild Avena species. Since thefirst reports of L. rigidum resistant to diclofop-methyl(Heap and Knight, 1982; 1986; 1990), at least two
thousand field populations have developed
resistance. Similarly, in laboratory experiments,(Matthews and Powles, unpublished) resistance todiclofop-methyl was selected in as little as three
generations from an initially susceptible population
following application of diclofop-methyl at
agriculturally-relevant rates.
Many of the L. rigidum biotypes selected with andresistant to diclofop-methyl do not contain a resistant
ACCase (Matthews et al., 1990; Holtum et al., 1991).
Extensive studies have been conducted with one
such biotype (SLR31) to identify the basis of nontarget site resistance. This biotype exhibits a modest
increase in the rate of diclofop-methyl metabolism(Holtum et al., 1991). The rate of metabolism of
diclofop-acid, the herbicidally-active form, occurs at
about 1.5 times the rate observed in a susceptible
biotype (Figure 1A). An increase in the rate of
metabolism of this order should provide, at least, lowlevel resistance to diclofop-methyl – however, theoverall contribution that metabolism makes todiclofop-methyl resistance in SLR31 is difficult toassess. A considerable proportion of the diclofop acid,about 20 percent in SLR31 and 30 percent insusceptible biotypes, remains un-metabolized even
192 h after treatment (Holtum et al., 1991).
The location of this remaining herbicide is not known,
however, we speculate that it has been sequesteredaway from the metabolizing enzymes, and the active
site (Holtum et al., 1991; Holtum et al., 1994). Not allof the metabolism products of diclofop-methyl in
L. rigidum have been identified, however, glucose
conjugates of both arylhydroxy diclofop and diclofopacid have been observed (Shimabukuro and Hoffer,
1991; Preston, unpublished). SLR31 produced more
glucose conjugates of arylhydroxy diclofop than did
the susceptible biotype (Preston, unpublished),suggesting the involvement of a Cyt P450 in theenhanced metabolism of diclofop in this biotype.
Despite these observations, in pot experiments thelevel of diclofop-methyl resistance in SLR31 is notaltered by the addition of the cytochrome P450
inhibitors 1-aminobenzotriazole (ABT), piperonyl
butoxide (PBO), or tetcyclasis (Tardif, Preston andPowles, unpublished). Differences in diclofop
metabolism between SLR31 and susceptible biotypes

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do not appear to be due to secondary differences
between herbicide affected and unaffected plants asother L. rigidum biotypes (SLR3 and WLR96) with
ACCase enzyme-based resistance to diclofop, show
no increase in diclofop metabolism (Tardif et al.,
1993; Tardif, Preston, Holtum and Powles,
unpublished). In addition, this biotype also displays amembrane recovery response whose relationship toresistance is uncertain (Häusler et al., 1991;
Shimabukuro and Hoffer, 1992). Studies to identify
the precise nature of non target site cross resistancein this biotype are continuing in our laboratory.
A number of biotypes of A. myosuroides exhibit
varying levels of resistance to diclofop-methyl andfenoxaprop-ethyl (Moss, 1992). Two biotypes, Peldon
A1 and Lincs. E1, from the U.K. have been examined
and are resistant to the APP herbicides diclofopmethyl and fenoxaprop-ethyl, and the CHD herbicide
tralkoxydim (Moss, 1990; Hall, Moss and Powles,
unpublished). Both resistant biotypes show enhanced
metabolism of diclofop-methyl and fenoxaprop-ethyl(Figure 3A). Rates of diclofop acid detoxification in theresistant biotypes (Peldon A1 and Lincs. E1) are 1.6
times faster than in the susceptible biotype (Hall,
Moss and Powles, unpublished). Similarly, the rate of
metabolism of fenoxaprop acid is about two times
faster in these two resistant biotypes compared to thesusceptible (Hall, Moss and Powles, unpublished).
These biotypes also show increased metabolism of
the substituted urea herbicides chlorotoluron (Figure3B) and isoproturon (Kemp and Caseley, 1987; Kemp
et al., 1990). It appears likely that enhanced
metabolism is the common mechanism of herbicide
resistance operating in the Peldon A1 biotype (Kempet al., 1990).
c. Non target site cross resistance toPS2-inhibiting herbicides
As discussed in Section 1, the vast majority of casesof herbicide resistance to the PS2-inhibiting
herbicides are the result of a change at the PS2 target
site, which confers resistance to the triazine andsome other PS2-inhibiting herbicides, but not to thesubstituted urea herbicides (Table 5). Conversely,
biotypes of L. rigidum in Australia have developed
resistance to PS2-inhibiting herbicides following
selection with either triazine or urea herbicides. A
decade of selection with atrazine (in a mixture withthe 1-4 triazole herbicide amitrole) resulted in abiotype (WLR2) resistant to atrazine and a wide rangeof other triazine herbicides (Burnet et al., 1992).
Significantly, this biotype exhibits cross resistance toa wide range of substituted urea herbicides (Burnet etal., 1992). Similarly, a L. rigidum biotype (VLR69)
selected for a decade with a substituted urea
herbicide (diuron) displays resistance to diuron which
also extends to a range of other urea herbicides andexhibits cross resistance to triazine herbicides (Burnet
et al., 1994b). The mechanism endowing triazine andsubstituted urea herbicide resistance has been
identified in these L. rigidum biotypes as due toenhanced rates of herbicide metabolism (Burnet etal., 1993a; b). In the resistant biotypes, the triazine
herbicide simazine is metabolized via N-dealkylation
to de-ethylsimazine and di-de-ethylsimazine at two to
three times the rate of metabolism attained by thesusceptible biotype (Figure 2A; Burnet et al., 1993a).
Lesser amounts of other metabolites are also
detected suggesting other degradation pathways arepresent. Similarly, the substituted urea herbicide
chlorotoluron is also metabolized at an enhanced rate
(Figure 2B; Burnet et al., 1993b). Although the firstmetabolite of chlorotoluron to appear is Nmonodemethylated chlorotoluron, the major
metabolite has been identified as a glucose conjugate
of ring-hydroxylated chlorotoluron (Preston,
unpublished). The resistant biotypes display
increased metabolism of chlorotoluron through both ofthese pathways suggesting the involvement of morethan one herbicide-detoxifying mechanism in thesebiotypes. Broad cross resistance to substituted urea
herbicides which have N-alkyl groups in common but
differ in phenyl substituents can be explained byincreased activity of an N-demethylating enzyme. The
ring-hydroxylating enzyme might then provide
increased resistance to some, but not all, substituted
ureas. Significantly, these resistant biotypes showmuch greater resistance to chlorotoluron, 8- to 10fold, than to other substituted urea herbicides, 2- to 3fold (Burnet et al., 1992; 1994b). ABT, PBO andtetcyclasis, three potent, broad-spectrum inhibitors of
Cyt P450 enzymes, inhibit metabolism ofchlorotoluron and antagonize resistance in these twobiotypes (Burnet et al., 1993b; Preston and Powles,
unpublished). ABT also inhibits simazine metabolism
and reduces the level of simazine resistance in thesebiotypes (Burnet et al., 1993a). Therefore, theenzymic basis for the enhanced metabolism
resistance mechanism in these biotypes is likely to be
due to increased activity of Cyt P450 monooxygenase
enzymes which have the capacity to either de-alkylate
or ring-hydroxylate these herbicides. However,despite intensive effort, it has not yet been possible toisolate from these biotypes active Cyt P450 enzymes
capable of metabolizing herbicides in vitro (Prestonand Powles, unpublished).
In Europe, biotypes of A. myosuroides havedeveloped resistance following selection with
substituted urea herbicides, particularly chlorotoluron.
As for L. rigidum, in all examined biotypes of
A. myosuroides resistant to substituted ureas,
resistance is not due to a resistant PS2 target site (DePrado et al., 1991; Hall, Moss and Powles,
unpublished). As with L. rigidum, resistance in
A. myosuroides is due to an enhanced rate of
metabolism of chlorotoluron and isoproturon (Figure
3B; Kemp et al., 1990; Hall, Moss and Powles,
unpublished), which is probably endowed byincreased activity of Cyt P450 catalyzed metabolism.

7

	
  

	
  

The level of resistance to chlorotoluron can be
reduced by adding a variety of Cyt P450 inhibitors
including ABT, triadimefon, and tridiphane (Kemp andCaseley, 1987; Kemp et al., 1990). Of these, ABT, atleast, can inhibit metabolism of chlorotoluron andisoproturon (Kemp and Caseley, 1991; Kemp et al.,1990). Direct evidence that a Cyt P450 enzyme is
responsible for resistance to chlorotoluron has
recently been obtained (J. Caseley, pers. comm.).
Microsomal membrane preparations isolated from
Peldon A1 and a susceptible population displayed low
intrinsic rates of chlorotoluron metabolism. Following
exposure of young seedlings to a low concentration ofchlorotoluron, the rates of metabolism in isolated
microsomes were increased, a process known as
induction. The rate of chlorotoluron metabolism by
isolated microsomes was greater for the resistantPeldon A1 biotype than for the susceptible.
It is clear from the abovementioned studies with
A. myosuroides and L. rigidum that a number of
biotypes have developed non target site crossresistance across many herbicide groups. The basisof non target site cross resistance is enhanced ratesof herbicide metabolism involving the Cyt P450
enzyme family. Control of such non target site crossresistant weed populations can be difficult withherbicides because Cyt P450 enzymes are able todetoxify a wide range of herbicidal compounds invitro (Moreland et al., 1993). Hence, any cropselective herbicide where selectivity is Cyt P450based is a likely candidate for non target site crossresistance. This means that existing metabolismbased resistant weed biotypes of L. rigidum andA. myosuroides are potentially resistant to yet-to-be
discovered herbicides that can be metabolized by Cyt
P450. While at the moment the only Cyt P450endowed non target site cross resistance reported
has been in L. rigidum and A. myosuroides, it is likelythat this phenomenon will appear in other weed
species.

III. Part B: Multiple Resistance to
Herbicides
The most intractable problems of herbicide resistance
now and for the future will involve weeds which exhibit
multiple herbicide resistance. Unknown in plants until
recently the phenomenon of multiple resistance isdefined as the expression (within individuals or
populations) of more than one resistance mechanism.
Multiple resistant plants may possess from two to
many distinct resistance mechanisms and may exhibit
resistance to a few or many herbicides. The simplest
cases are where an individual plant (or population)possesses two or more different resistancemechanisms which provide resistance to a single
herbicide, or class of herbicides. More complicatedare situations where two or more distinct resistancemechanisms have been selected either sequentiallyor concurrently by different herbicides and endow

resistance to the classes of herbicide to which they
had been exposed. The most complicated and difficult
to control situations are where a number of resistancemechanisms, involving both target site and non target
site resistance mechanisms, are present within thesame individual. Simple cases of multiple resistancehave been documented for a small number of weed
species, however, the majority of cases and the mostcomplicated situations have been reported forbiotypes of L. rigidum.
There are a small number of documented cases
where a weed biotype has resistance to a single classof herbicides but possesses two different resistancemechanisms. A triazine-resistant biotype ofBrachypodium distachyon with a resistant PS2 target
site also displayed increased metabolism of atrazine(Gressel et al., 1983). A biotype of L. rigidum (WLR1)
selected only with chlorsulfuron is resistant to ALSinhibiting herbicides and has a resistant ALS enzyme
as well as enhanced metabolism of chlorsulfuron(Christopher et al., 1992). Although both target site
and non target site cross resistance mechanisms arepresent in this biotype, resistance only extends to the
ALS-inhibiting herbicides. In both of these cases, themodified target site is the most powerful resistancemechanism. As researchers frequently examine fortarget site based resistance mechanisms early in astudy, we believe it likely that there have been manycases reported as target site mechanisms without
examination for the presence of other resistancemechanisms. This is understandable in that target
site-based resistance is often more efficacious thannon target site mechanisms and tends to obscure thelatter when present in the same individual.
A somewhat more complicated case of multiple
herbicide resistance occurs in a biotype of A.
myosuroides (Lincs. E1). This biotype has widespread
non target site cross resistance endowed byincreased metabolism to a range of herbicide classes
following selection with chlorotoluron (Hall, Moss andPowles, unpublished). Following additional selection
with an ACCase herbicide, in addition to enhanced
herbicide metabolism, this biotype has individuals(approximately 15 percent of the population) withresistant ACCase (Hall, Moss and Powles,
unpublished). Similarly, multiple herbicide resistancehas been reported on a number of occasions whenherbicides of different chemical classes have been
applied to a weed population either as a mixture, orsequentially, following the development of resistanceto the first herbicide. At least one biotype of Conyza
canadensis from Hungary displays multiple
mechanisms of resistance. This biotype has aselection history involving atrazine and paraquat andis resistant to both triazine and bipyridyl herbicides(Pölös et al., 1988). Resistance to the triazine
herbicides, as in most cases of triazine resistance, isconferred by a change at the PS2 active site (Pölös etal., 1987). Resistance to paraquat is due to a non-

8

	
  

	
  

target site mechanism, which has not yet been
identified (Lehoczki et al., 1992). Similarly, a biotype
of Amaranthus retroflexus developed target site
resistance to triazine herbicides following many years
of application. Diuron was then applied to thisresistant population and resistance developed todiuron through another, as yet unknown, mechanism(Lehoczki et al., 1991). In this case the accumulationof resistance mechanisms was sequential. A biotypeof Phalaris paradoxa with PS2 target site-based
resistance to triazine herbicides was also reported tobe resistant to diclofop-methyl (Yaacoby et al., 1986).
In this case, no history of exposure to diclofop-methyl
was reported and the mechanism of cross resistanceto diclofop-methyl has not been examined. Fromthese few studies it is clear that resistance can occur
to herbicide mixtures, and that in such cases, multiple
mechanisms of resistance may appear.
The most complicated and intractable cases ofmultiple resistance to herbicides have been reported
in L. rigidum in Australia. As presented in Table 1,many L. rigidum populations possess multiple
resistance mechanisms and individuals within any
population may differ in their component resistancegenes. Studies with L. rigidum biotype SLR31 present
the best documented case of resistance conferred bymultiple mechanisms. SLR31 has a complex history
of applications of many different herbicides and isresistant to herbicides from many different classes(Table 1). This biotype exhibits multiple resistancedue to the following resistance mechanisms:1)

a 1.5-fold enhanced metabolism of the
ACCase-inhibiting herbicide diclofopmethyl (Figure 1A; Holtum et al., 1991)2)

the membrane recovery response
correlated with resistance to ACCaseinhibiting herbicides (Häusler et al., 1991)

3)

12 percent of the population possess
herbicide-resistant ACCase enzyme(Tardif and Powles, 1994), with theremainder of the resistant population
containing a herbicide-sensitive ACCase(Matthews et al., 1990)

4)

a twofold enhanced metabolism of the
ALS-inhibiting herbicide chlorsulfuron(Figure 1B; Christopher et al., 1991; 1992)

Another L. rigidum biotype, VLR69, has also been
exposed to a wide variety of herbicides over a 20-year
period and has similarly developed multiple herbicide

resistance (Table 1) and possesses multiple
resistance mechanisms:1)

a 1.5-fold enhanced metabolism of the
ACCase-inhibiting herbicide diclofopmethyl (Preston, Tardif, Christopher andPowles, unpublished)2)

all, or the vast majority of individuals
possess a resistant form of ACCase
enzyme (Preston, Tardif, Christopher andPowles, unpublished)3)

a twofold enhanced metabolism of the
ALS-inhibiting herbicide chlorsulfuron(Figure 2C; Burnet et al., 1994a)

4)

5 percent of the population exhibits an
ALS enzyme resistant to ALS-inhibiting
herbicides with the remainder of the
population possessing a susceptible ALS(Burnet et al., 1994a)5)

the membrane-recovery phenomenon(Häusler et al., 1991)

6)

enhanced metabolism of the PS2inhibiting herbicides simazine andchlorotoluron (Figure 2A and 2B; Burnet etal., 1993a; b)

Therefore, biotype VLR69 contains a number ofresistance mechanisms, including resistant ALS,
resistant ACCase, and enhanced metabolism. The
enhanced metabolism evident for ACCase-, ALS- andPS2-inhibiting herbicides is unlikely to be endowed by
one enzyme as recent evidence based on the effectsof Cyt P450 inhibitors on metabolism of a variety ofherbicides suggests that several Cyt P450 enzymes
are responsible for metabolism-based crossresistance in this biotype (Preston, Tardif, Christopher
and Powles, unpublished).
One conclusion that can be drawn from the studies on
multiple resistance in L. rigidum is that biotypes withextremely varied and persistent histories ofapplication of selective herbicides have developed
widespread multiple resistance as the result of theaccumulation of many resistance mechanisms.
Biotypes with less varied herbicide histories typicallyhave only one or two resistance mechanisms. A likely
scenario is that multiple resistance can develop if
alternative selective herbicides are employed as the

9

	
  

	
  

sole means of control of already resistant populations.
Therefore, integrated weed management (IWM)
strategies are required. For Southern Australian
agriculture we are in the middle of a 6-year agronomic
research project to quantify IWM practices for thecontrol of herbicide resistant Avena spp. andL. rigidum populations (Matthews, Lwellewyn,
Nietschke, Reeves and Powles, unpublished). Whileoutside the scope of this review it is clear that there
are a range of weed control techniques which can be
integrated with herbicide use to deliver IWM programsfor L. rigidum control that are economically andenvironmentally sustainable. As reviewed by
Matthews (1994), crop and pasture rotation to
reduce L. rigidum seedbank reserves, together withmanipulation of agronomic factors and judicious
herbicide usage can produce a workable IWM
package. In the case of L. rigidum, the mature seedremains rigidly attached to the plant at maturity andtherefore innovations involving modification of crop
harvesting machinery enables substantial L. rigidum
seed to be retained and removed in the harvest
operation (Matthews et al., 1994). This practice cangreatly reduce L. rigidum seed return to fields andcontribute to a successful IWM strategy (Matthews,
1994).

IV. Conclusions and Future Directions
As discussed in Part A of this review, by far the mostcommon forms of cross resistance to herbicides areconferred by target site cross resistance mechanisms.
Target site changes only endow resistance toherbicides affecting a target site. As detailed in Tables
3-5, there can be quite different patterns and degreeof target site cross resistance across chemical groups
affecting a target site. From a practical viewpoint,
control of target site-based resistant weed populations
can often easily be achieved by the use of herbicides
with a different mode of action. This has been themost widely used method for combating target site
based herbicide resistance. The success with whichtarget site-based resistance has been controlled byalternative herbicides has led to a certain
complacency as to the ease with which herbicideresistant populations can be managed. However, theappearance of non target site-based cross resistantweed populations, with wide ranging herbicide
resistance spectra, should thoroughly dispel the
notion that herbicide rotation alone will manage
resistance. For example, as discussed in Section 2,
resistance due to increased metabolism in many
biotypes of L. rigidum and A. myosuroides means
resistance across numerous herbicide classes giving
widespread cross resistance (Tables 1 & 2). In thesecases of non target site cross resistance endowed bymetabolism, the Cyt P450 enzyme family have been
implicated. To date, Cyt P450-based metabolism isthe only mechanism documented to give widespreadcross resistance in weeds and control of such
populations can be difficult as Cyt P450 enzymes areable to detoxify a wide range of herbicidal
compounds. In L. rigidum, the enhanced metabolism
Cyt P450 resistance mechanism is often combinedwith other resistance mechanisms resulting inbiotypes with multiple resistance mechanisms
conferring resistance across many herbicide
chemistries (Part B).
While L. rigidum in Australia is currently unique in therange of multiple resistance mechanisms
accumulated, herbicide resistance in A. myosuroides
and other species illustrates that non target site crossresistance and the accumulation of resistancemechanisms within populations will occur in otherspecies. One lesson learned from L. rigidum inAustralia is that it is those populations with the mostintense and varied herbicide selection pressure thatare most likely to exhibit multiple resistancemechanisms. We should not be surprised that a
species such as L. rigidum possesses multiple
resistance mechanisms (Powles and Matthews,
1992). This cross-pollinated, highly abundant andgenetically variable annual species is present inAustralia over vast areas where it is regularly exposedto herbicides. This selection pressure has led to theaccumulation of a diversity of resistance mechanisms,
both target site and non target site, resulting in aformidable array of resistance mechanisms. Hence,
multiple resistance has first occurred in L. rigidum
because of the confluence of the biology of Lolium
and its abundance and role in the Australian agroecosystem (Powles and Matthews, 1992).
The lessons to be learned from the Australianexperience with L. rigidum are salient; with current
herbicide use patterns, other weed species in various
parts of the world will inevitably exhibit multiple
resistance. Once multiple herbicide resistance ismanifest, especially where one of the resistancemechanisms is Cyt P450-endowed non target site
cross resistance, herbicide control can be difficult andeven new herbicide chemistries may be unsuccessful
on existing multiple resistant biotypes. As weed
control is essential to agricultural productivity tosustain a burgeoning world population, it is vital that
there not be large scale development of multiple
herbicide-resistant weed populations in major foodproducing areas. To delay, avoid or combat
widespread herbicide resistance, all sectors of the
agricultural industry must learn to advocate and use
herbicides with restraint within IWM strategies which
minimize the selection pressures for resistance.
Biological and evolutionary realities dictate that this is
the only sensible way forward. We must accept thatmodern herbicides are scarce resources of great
utility in aiding food and fiber production and that theyshould be used wisely so as to ensure that they are
not driven into redundancy by resistance. Giveneconomic realities, at both the manufacturer andproducer level, there are considerable challenges inchanging current practice. It is hoped that this review

10

	
  

	
  

stimulates thought and action towards the essentialchanges needed.

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Figure 1. Enhanced
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from Holtum et al.,1991 and Christopher
et al., 1992

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Figure 2. Enhanced
metabolism of simazine(A), chlorotoluron (B),and chlorsulfuron (C)in L. rigidum biotype
VLR69 (J) compared to asusceptible biotype (E).
Data are modified from
Burnet et al., 1993a;
1993b; 1994a.

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Yaacoby, T., M. Schonfeld, and B. Rubin. 1986.
Characteristics of atrazine resistant biotypes of three grass
weeds. Weed Sci. 34: 181-184.

	  Figure 3. Enhanced
metabolism of diclofop(A) and chlorotoluron (B)in A.
myosuroides biotype
Peldon A1 (J) compared
to a susceptible biotype(E). Data are modified
from Hall, Moss andPowles, unpublished.

15

	
  

	
  

TablesTable 1. Herbicide-Resistant Biotypes of L. rigidum Mentioned in the Text: Resistance Status andMechanisms.
BiotypeResistance Status(chemical classes)

Resistance Mechanisms Identified

References

Resistant ACCase

Tardit et al., 1993

Aryloxyphenoxypropionate
SLR3
Cyclohexanedione
Aryloxyphenoxypropionate
Cyclohexanedione
Holtum et al., 1991
Sulfonylurea

Resistant ACCase

Imidazolinone

Metabolism

Dinitroanaline

Membrane repolarisation

Häusler et al., 1991
SLR31

Tardif & Powles, 1994
Christopher et al., 1991
Chloracetamide
Isoxazolidinone
Carbamate
Aryloxyphenoxypropionate
Cyclohexanedione
Burnet et al., 1993a
Sulfonylurea

Resistant ACCase

Imidazolinone

Resistant ALS

Triazine

Metabolism

Substituted urea

Membrane repolarisation

Burnet et al., 1993b
VLR69

Burnet et al., 1994a
Häusler et al., 1991
Preston, Tardif, Christopher & Powles, unpublished
Triazinone
Chloroacetamide
Sulfonylurea

Resistant ALS

Imidazolinone

Metabolism

WLR1

Christopher et al., 1992

Triazine
Substituted urea
WLR2

Burnet et al., 1993aMetabolism

Triazinone

Burnet et al., 1993b

Aminotriazole
Aryloxyphenoxypropionate

Resistant ACCase

Häusler et al., 1991

Cyclohexanedione

Membrane repolarisation

Holtum & Powles, unpublished

WLR96

a: Biotypes are not necessarily resistant to all members of each herbicide class.
b: Mechanisms indicated may give resistance to one or more herbicide classes. See text for further details.

16

	
  

	
  

Table 2. Herbicide-Resistant Biotypes of A. myosuroides Mentioned in the Text: Resistance Status andMechanisms.
BiotypeResistance Status(chemical classes)

Resistance Mechanisms Identified

References

Aryloxyphenoxypropionate
Cyclohexanedione

Resistant ACCase

Substituted urea

Metabolism

Lincs. E1

Hall, Moss & Powles, unpublishedDinitroanaline
Aryloxyphenoxypropionate

Mason

Resistant ACCase

Hall, Moss & Powles, unpublished

Resistant ACCase

Hall, Moss & Powles, unpublished

Cyclohexanedione

Aryloxyphenoxypropionate
OtmoorCyclohexanedione
Aryloxyphenoxypropionate
Cyclohexanedione
Substituted urea
Triazine
Kemp & Caseley, 1987
Triazinone
Peldon A1

Metabolism

Kemp et al., 1990

Sulfonylurea
Hall, Moss & Powles, unpublished
Imidazolinone
Dinitroanaline
Thiocarbamate
Carbamatea: Biotypes are not necessarily resistant to all members of each herbicide class.

	
  

17

	
  

	
  

Table 3: Target Site Cross Resistance Patterns of ALS from Weed Species Resistant to ALS-inhibiting
Herbicides
Species - biotype

Herbicide

Reference

Sulfonylurea(Chlorsulfuron)

Imidazolinone(Imazapyr)

Triazolopyrimidine(2,6-Dichlorosulfonanilide)

Resistance ratio (I50 R / I50 S)
Brassica tournefortii

>95

0.8

>8 (Flumetsulam)

Boutsalis & Powles, unpublished

Kochia scoparia

18

6

20

Saari et al., 1990

Lolium perenne

35

7

>24

Saari et al., 1992

Lolium rigidum - WLR1

>32

8

-

Christopher et al., 1992

Salsola iberica

8

4

8

Saari et al., 1992

Sisymbrium orientale

>190

75

>14 (Flumetsulam)

Boutsalis & Powles, unpublished

Sonchus oleraceus

14

3

3 (Flumetsulam)

Boutsalis & Powles, unpublished

Stelleria media

132

9 (Flumetsulam)

Saari et al., 1992

Stelleria media>54

7 (Imazamethabenz)>100

Hall & Devine, 1990

Xanthium strumarium

1.1 (Chlorimuron)>324 (Imazaquin)

1.4 (Flumetsulam)

Schmitzer et al., 1993

Table 4: Target Site Cross Resistance Patterns of ACCase from Weed Species Resistant to ACCase-inhibiting
Herbicides
Aryloxyphenoxypropionate

Cyclohexanedione(Diclofop)(Sethoxydim)(Haloxyfop)

Resistance ratio (I50 R / I50 S)
Alopecurus myosuroides - Mason

11>27 (Fenoxaprop)>12

Hall, Moss & Powles, unpublished

Alopecurus myosuroides - Otmoor

14>36 (Fenoxaprop)>12

Hall, Moss & Powles, unpublishedAvena fatua

10

7

14

Maneechote, Preston & Powles, unpublishedAvena sterilis

52

25

8

Maneechote et al., 1994

Lolium multiflorum

28

9

0.9

Gronwald et al.,1992

Lolium rigidum – SLR3

>35

>10

7.8

Tardif et al., 1993

Lolium rigidum – WLR96

85

216

2.8

Holtum & Powles, unpublished

Lolium rigidum – VLR69

30

20

1

Preston, Tardif, Christopher & Prowles,
unpublished

Setaria viridis>47

60 (Quizalofop)

50

Marles, et al., 1993, unpublished

18

	
  

	
  

Table 5: Target Site Cross Resistance Patterns of PS2 from Weed Species Resistant to PS2-inhibiting
Herbicides
Species

Herbicide
Triazine(Atrazine)

Reference
Triazinone(Metribuzin)

Uracil(Bromacil)

Pyridazinone(Pyrazon)

Substituted Urea
(Diuron)Resistance ratio (I50 R / I50 S)
Amaranthus hybridus

830

260

20

290

1.4

Fuerst et al., 1986

Amaranthus retroflexus

~1000

260

20

~63

1.4

Pfister & Arntzen, 1979

Amaranthus retroflexus

251

>1500

>2000

-

4

Oettmeier et al., 1982

Ambrosia artemisiifolia

189

21

-

-

1.9

Arntzen et al., 1982

Brassica campestris

1000

89

9

-

1.7

Ducruet & De Prado, 1982

Chenopodium album

1300

33

88

330

-

Fuerst et al., 1986

Chenopodium album

542

167

-

-

1.2

De Prado et al., 1989

Conyza bonariensis

407

91

-

-

1.1

De Prado et al., 1989

Senecio vulgaris

>200

-

125

-

1.6

Radosevich et al., 1979

Senecio vulgaris

890

-

114

16

1.6

Fuerst et al., 1986

.

19