Pest Management Science
Pest Manag Sci 61:301–311 (2005)
DOI: 10.1002/ps.1015
Herbicide-resistant crops and weed resistance
to herbicides†
Micheal DK Owen∗ and Ian A Zelaya
Iowa State University, Ames, IA 50011-1011, USA
Abstract: The adoption of genetically modified (GM) crops has increased dramatically during the last
3 years, and currently over 52 million hectares of GM crops are planted world-wide. Approximately
41 million hectares of GM crops planted are herbicide-resistant crops, which includes an estimated
33.3 million hectares of herbicide-resistant soybean. Herbicide-resistant maize, canola, cotton and
soybean accounted for 77% of the GM crop hectares in 2001. However, sugarbeet, wheat, and as many
as 14 other crops have transgenic herbicide-resistant cultivars that may be commercially available in
the near future. There are many risks associated with the production of GM and herbicide-resistant
crops, including problems with grain contamination, segregation and introgression of herbicide-resistant
traits, marketplace acceptance and an increased reliance on herbicides for weed control. The latter issue
is represented in the occurrence of weed population shifts, the evolution of herbicide-resistant weed
populations and herbicide-resistant crops becoming volunteer weeds. Another issue is the ecological
impact that simple weed management programs based on herbicide-resistant crops have on weed
communities. Asiatic dayflower (Commelina cumminus L) common lambsquarters (Chenopodium album
L) and wild buckwheat (Polygonum convolvulus L) are reported to be increasing in prominence in some
agroecosystems due to the simple and significant selection pressure brought to bear by herbicideresistant crops and the concomitant use of the herbicide. Finally, evolution of herbicide-resistant weed
populations attributable to the herbicide-resistant crop/herbicide program has been observed. Examples
of herbicide-resistant weeds include populations of horseweed (Conyza canadensis (L) Cronq) resistant
to N-(phosphonomethyl)glycine (glyphosate). An important question is whether or not these problems
represent significant economic issues for future agriculture.
 2005 Society of Chemical Industry
Keywords: genetically modified crops; glyphosate; herbicide resistance; herbicide tolerance; interspecific
hybridization; weed population shifts
1 INTRODUCTION
The adoption of transgenic herbicide-resistant crops
has increased dramatically in the last decade. Most
of the increase in hectares of transgenic crops planted
is attributable to glyphosate-resistant soybean, maize,
canola and cotton. Glyphosate-resistant soybean and
canola were introduced in 1996, cotton in 1997, and
maize in 1999. Glyphosate-resistant cotton accounts
for 56% of the cotton hectares planted in the USA
in 2001.1 In 2001, glyphosate-resistant soybean and
maize cultivars accounted for over 70 and 10%,
respectively, of the hectares planted in the Mid-west
USA and the adoption trend is increasing (Fig 1).2 In
Argentina, glyphosate-resistant soybean accounts for
98% of the hectares planted in 2001.3 The results of
this unprecedented change in agriculture have been
many, but perhaps most dramatic is the simplification
of weed-control tactics; growers can now apply a
single herbicide (glyphosate) at elevated rates of active
ingredient and at multiple times during the growing
season without concern for injury to the crop. While
a number of agriculturalists and economists suggest
that the adoption of herbicide-resistant crops will
reduce herbicide use dramatically, others suggest that
herbicide use will actually increase.4 – 6 Regardless,
the number of herbicides applied has declined, thus
increasing the ecological implications such as reducing
the biodiversity of arable land, facilitating population
shifts in weed communities and the evolution of
herbicide-resistant biotypes.7 – 10
Historically, a number of significant changes in agricultural systems have occurred with significant impact
on weed communities. Adoption of conservation
tillage practices and concomitant changes in herbicide
use in the 1980s resulted in more small-seeded annual
weeds.11 The development and commercialization of
∗
Correspondence to: Micheal DK Owen, 2104 Agronomy Hall, Iowa State University, Ames, IA 50011-1011, USA
E-mail: mdowen@iastate.edu
† Paper presented at the Symposium ‘Herbicide-resistant crops from biotechnology: current and future status’ held by the Agrochemicals
Division of the American Chemical Society at the 227th National Meeting, Anaheim, CA, 29–30 March, 2004, to mark the presentation of
the International Award for Research in Agrochemicals to Dr Stephen O Duke.
(Received 13 September 2004; revised version received 16 November 2004; accepted 23 November 2004)
Published online 25 January 2005
 2005 Society of Chemical Industry. Pest Manag Sci 1526–498X/2005/$30.00
301
MDK Owen, IA Zelaya
3500
400
350
300
area treated (%)
AE glyphosate (mg) applied per year
450
AE glyphosate (mg) applied per year
500
250
maize
50
45
40
35
30
25
20
15
10
5
0
10
4 5
8 8
6
9 7 10
10 10
200
150
100
50
y = 2.52-94 × (1.12)x
R2 = 0.67
3000
2500
2000
area treated (%)
0
100
90
80
70
60
50
40
30
20
10
0
9 10
7
soybean
9
7
3
6
5
8
7
7
10
1500
1000
500
0
y = 7.54-236 × (1.31)x
R2 = 0.94
1990 1991 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001
Growing season
Figure 1. Glyphosate use in maize and soybean within US Mid-west
states (IL, IN, IA, KS, MI, MN, MO, NE, OH, WI). Fit of the exponential
growth model (y = abx ) to the data is indicated by the discontinuous
lines. Inserts: mean percentage area treated with glyphosate among
states. Circles or bars represent the mean of states as indicated by
the number above bars in inserts; extensions on circles or bars
denote 95% confidence intervals associated with the mean. Data
were compiled from the US Department of Agriculture (USDA)
National Agricultural Statistics Service (NASS) database.
herbicides that inhibit acetolactate synthase (ALS, EC
2.2.1.6) resulted in another significant change in weed
communities and ushered in the widespread problems
with common waterhemp (Amaranthus tuberculatus
(Moq) Sauer) and the evolution of herbicide-resistant
biotypes.12 The question that must be addressed is
whether or not the most recent major change in agroecosystems, the adoption of herbicide-resistant crops,
represents a different risk than previous changes. The
scope of this paper will be limited to herbicide-resistant
crops resulting from transgenic incorporation of traits,
and the implications on weed communities. While
other issues exist with the adoption of transgenic
herbicide-resistant crops (eg consumer fears about
food safety), discussions about these issues will not be
addressed and the reader is directed to other sources
of information.3,13 – 16
2 WEED POPULATION SHIFTS
Agroecosystems impart selection pressure on weed
communities that inevitably result in weed population
shifts.17 A weed population, once introduced into the
seedbank, will rise in prominence within the weed
community when selection pressure (disturbance)
302
that favors that species is imparted upon the
agroecosystem.18 The most important selective forces
on a weed community in an agroecosystem are the
tillage and herbicide regimes. The adoption of HR
crops will result in greater selection pressure on
the weed community due to a limited number of
different herbicides used. Increased selection pressure
will increase weed population shifts.19,20 Selection
pressure imparted by herbicide tactics can result in
weed shifts attributable to the natural resistance of
a particular species to the herbicide or the evolution
of herbicide resistance within the weed population.
Both of these types of weed shift have occurred
in response to grower adoption of crop production
systems based on a herbicide-resistant crop and the
resultant application of the herbicide.
2.1 Ecological adaptation
Weed shifts can be attributable to general ‘ecological
adaptation’ of the weed population to the tactics used
in crop production. A long-term study demonstrated
that different tillage systems caused different weed
population shifts, and no-tillage caused the most rapid
and dramatic shift in the weed community.21 Woolly
cupgrass (Eriochloa villosa (Thunb) Kunth) is an
excellent example of a weed shift attributable primarily
to ecological adaptation due to a number factors
such as opportunistic germination habit, fecundity,
competitive ability and adaptation to conservation
tillage systems.17 Woolly cupgrass is particularly
difficult to manage in maize and soybean, regardless
of the management tactics used, and while growers
suspect evolved herbicide resistance within specific
woolly cupgrass populations, no evidence of resistance
has been obtained and control failures represent,
in general, inadequate management on the part of
growers.22
With the recent widespread adoption of glyphosateresistant crops, considerable research has been
undertaken to determine whether changes in weed
populations occurred in response to the selection
pressure imparted by the crop production system.
Not surprisingly, weed diversity in glyphosateresistant soybean was a factor of the number of
glyphosate applications per season and geographic
location.23 Single glyphosate applications had higher
weed species diversity than any management tactic,
including the untreated control. Presumably, the
increased weed species diversity was attributable to the
single glyphosate application controlling the dominant
species, thus providing an ecological opportunity to
other species. If two glyphosate applications were used,
weed species diversity was low, even when compared
with residual herbicide systems. Weed species diversity
also increased for southern locations.
Weed diversity can be a function of weed population
density, and, presumably, the lower the population
density and diversity, the greater the selection
pressure for weed shifts. Weed population density
declined for multiple glyphosate applications and
Pest Manag Sci 61:301–311 (2005)
Herbicide-resistant crops and weed resistance to herbicides
supplemental inter-row cultivation, compared with
soil-applied residual herbicides.24 However, risks for
weed population shifts for weed management based on
continuous glyphosate-resistant crops and glyphosate
were assessed to be no greater than those associated
with other herbicides and conventional crops. Other
researchers suggested that the selection pressure from
continuous glyphosate applications to glyphosateresistant crops would result in significant shifts in weed
populations.25 Furthermore, it was suggested that
the weed seedbank for those adapted species would
increase dramatically.26 The mechanisms by which
weed shifts occurred in the glyphosate-based systems
were natural resistance to glyphosate [ie morningglory
(Ipomea spp)] and by avoidance due to differential
emergence patterns (ie woolly cupgrass).26,27
2.2 Evolved resistance
Numerous (174) weed species have evolved resistance
to a number of herbicides in many, if not most,
agroecosystems.28 There are 291 resistant biotypes
reported. Most of the resistant biotypes evolved
without the selection pressure resulting from the
adoption of herbicide-resistant crops. However, with
glyphosate-resistant crops being widely adopted, and
the applications increasing (Fig 1), it is argued that the
evolution of herbicide-resistant weed populations will
escalate rapidly.17 There appear to be two important
mechanisms by which resistance can evolve. One,
and perhaps most widely documented, is targetsite resistance (ie monogenic) where high rates of
a herbicide have been applied.22 The other has
been labeled ‘creeping resistance’ (ie polygenic) and
is attributable to reduced herbicide rates.29 The
first mechanism accounts for many of the currently
identified herbicide-resistant biotypes such as those
resistant to ALS-inhibiting herbicides. The second
mechanism is suggested to describe the current
situation with specific weeds evolving resistance to
glyphosate where the mechanism is likely to include
multiple genes. Given the inevitability of evolved
herbicide resistance, it is important to consider
tactics to deter or delay the development of resistant
populations. Several strategies have been proposed
that may effectively impact the evolution of herbicide
resistance: the alternation of low and high herbicide
rates, the rotation of herbicides with different modes of
action, or the use of herbicides in combination.30 The
latter has been modeled and appears to substantially
delay herbicide resistance when compared with the
rotation of herbicides.31 Below is a brief update of
currently important herbicides and cases of evolved
resistance in relation to the adoption of herbicideresistant crops.
2.2.1 ALS-inhibiting herbicides
The evolution of resistance to ALS-inhibiting herbicides has been widespread in agroecosystems where
these herbicides are used. The adoption of herbicideresistant crops, particularly glyphosate-resistant crops,
Pest Manag Sci 61:301–311 (2005)
had little direct impact on the widespread evolution of ALS-inhibiting-herbicide resistance. However,
ALS-inhibiting-herbicide resistance likely fueled the
adoption of herbicide-resistant crops because growers
determined that control of the resistant biotypes would
be better with glyphosate-based systems. Approximately 86 weed species have evolved resistance to
individual or multiple ALS-inhibiting herbicides and
most reported species have several different biotypes
reported.28 Furthermore, interspecific hybridization
of some species is reported and given the pollen
transport of the resistance trait in combination with
the selection pressure from weed management tactics, ALS-inhibiting-herbicide resistance has spread
rapidly through many agroecosystems and provides
some insight as to the potential introgression of transgenic traits from open-pollinated herbicide-resistant
crops and related weed species.32 – 34
2.2.2 PPO-inhibiting herbicides
The evolution of protoporphyrinogen oxidase (PPO,
EC 1.3.3.4) inhibiting herbicide resistance in weed
populations was not attributable to the adoption of
herbicide-resistant crops, but was in part, the result
of evolved resistance to ALS-inhibiting herbicides.
Currently, there are two weed species that are reported
to be resistant to PPO-inhibiting herbicides.28 Wild
poinsettia (Euphorbia heterophylla L) populations in
Brazil were reported resistant to a number of
PPO-inhibiting herbicides as well as a number
of ALS-inhibiting herbicides. Common waterhemp
populations in Illinois and Kansas were also reported
to demonstrate multiple resistance, but at the current
time this is a limited problem. Common waterhemp
populations evolved resistance to PPO-inhibiting
herbicides due to growers using this class of herbicides
to control the ALS-resistant populations.35 The
evolution of PPO resistance is important to growers
who adopt glyphosate-resistant soybean, as glyphosate
has not consistently controlled all weeds within
the agroecosystem. Anecdotal reports suggest that
glyphosate is frequently supplemented with a PPOinhibiting herbicide, so that evolved resistance to PPOinhibiting herbicides would impact the effectiveness of
glyphosate.
2.2.3 HPPD-inhibiting herbicides
To date, no resistance to 4-hydroxyphenylpyruvate
dioxygenase (HPPD, EC 1.13.11.27) inhibiting
herbicides has been reported.28 It is unlikely that
crops resistant to HPPD-inhibiting herbicides will be
commercialized in the near future, so that HPPDresistant crops will not directly enhance evolution of
resistance to this herbicide family. However, given
the evolved resistance to glyphosate, it is possible
that HPPD-inhibiting herbicides will be used more
frequently. It is conceivable that the inclusion of
a HPPD-inhibiting herbicide to supplement weed
control in a herbicide-resistant crop could provide
sufficient selection pressure to cause the evolution
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MDK Owen, IA Zelaya
of a herbicide-resistant weed population. Thus, the
adoption of an herbicide-resistant crop could indirectly
impact the evolution of HPPD resistance in weeds.
2.2.4 Glyphosate
The evolution of resistance to glyphosate has been
aggressively debated for a number of years. Many
weed scientists from the public sector felt strongly,
and agreed adamantly with the position proposed by
the agrochemical industry, that because of the unique
site of action and the general lack of metabolism in
target species, resistance to glyphosate would evolve
slowly.36,37 Other weed scientists, however argued
that the genetic adaptability of weed populations
and the severe selection pressure that would be
imposed on the agroecosystems would result in
glyphosate-resistant populations. It was suggested that
there were fewer constraints on the evolution of
glyphosate resistance than originally proposed, and
it was predicted that resistance in weeds would
evolve.38 Arguments also indicated that not only
would the evolution of glyphosate resistance be an
issue, but also weed populations shifts would occur
in response to the adoption of glyphosate-resistant
crops.39 Evolved glyphosate resistance was identified
in horseweed (Conyza canadensis (L) Cronq) 3 years
after the adoption of glyphosate-resistant soybean.40
The issues surrounding glyphosate-resistant crops
have resulted in the termination of some promising
production opportunities. Despite these hurdles,
research continues, and a promising new transgene
has been announced that confers a different source of
glyphosate resistance for crops.41 The need for other
tactics to manage weeds will continue regardless and,
according to the author, likely escalate in the very
near future due to the impact of glyphosate-resistant
crops.11,39 A brief review of current of glyphosateresistant weed populations follows.
2.2.4.1 Lolium species
Glyphosate resistance in Lolium spp is a problem, and
research has been conducted on the subject. Early
publications suggested that Lolium spp had consider
propensity to evolve resistance to herbicides.42 Resistance to glyphosate was reported in the late 1990s by
several research groups, but early investigations did not
conclude any specific mechanism of resistance.43,44
Rigid ryegrass (L rigidum (Gaud)) was reported to
have high levels of resistance to numerous herbicides including acetyl-CoA carboxylase (ACCase, EC
6.4.1.2) and ALS-inhibiting herbicides.45 Multiple
resistance to herbicides was observed in over 30%
of the populations sampled and it was concluded that
herbicide-resistant populations of rigid ryegrass were
more common than susceptible populations. Some
rigid ryegrass populations demonstrated that the multiple herbicide resistance was based on several genes.46
The importance of this background, with regard to the
evolution of resistance to glyphosate, is that Lolium
spp appear to be prone to evolving herbicide resistance
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and are reported to have several mechanisms by which
resistance evolves (eg metabolism or modified target site). Resistance to glyphosate was reported after
15 years of repeated applications in a specific cropping system in Australia.44 The level of resistance
was reported to be 7- to 11-fold compared with the
susceptible rigid ryegrass population.
The mechanism of resistance is still not completely described, despite the efforts of several
research groups. Glyphosate uptake, translocation
and metabolism were initially ruled out as possible mechanisms, but more recent reports suggest
that differential cellular translocation of glyphosate
is implicated in resistance.47,48 In the susceptible rigid
ryegrass, glyphosate accumulated in the root tips while
in resistant biotypes accumulation occurred in the
leaf tips. Yet glyphosate resistance in the Australian
rigid ryegrass is monofactorial, incompletely dominant, and the allele governing resistance is located
in the nuclear genome.49 Research on a California
rigid ryegrass biotype ruled out differential absorption and distribution of glyphosate as the potential
mechanisms of resistance, but a 10-fold increase
in shikimate was observed in the sensitive biotypes
compared with the resistant biotypes.50 Nevertheless, differences in shikimate levels or sensitivity to
glyphosate did not explain the differential responses
of the rigid ryegrass biotypes. More recently, no difference in the intercellular glyphosate transport to
the chloroplast was observed between susceptible
and resistant rigid ryegrass plants; however, the 3phosphoshikimate 1-carboxyvinyltransferase (EPSPS)
of susceptible plants was more sensitive to glyphosate.
Inheritance of glyphosate resistance in the California
rigid ryegrass biotype is apparently governed by more
than one gene.51
Italian ryegrass (L multiflorum Lam) has evolved
glyphosate resistance in Chilean fruit orchards after
8–10 years of use.52 Like rigid ryegrass populations in
Australia, differential absorption, translocation, and
allocation of glyphosate were not identified as the
cause of resistance.53 In all of these reported cases, the
selection pressure imposed on the agroecosystem did
not involve a transgenic crop. It is presumed that the
adoption of glyphosate-resistant crops would result
in greater selection pressure on the rigid ryegrass
populations with glyphosate and thus increase the
likelihood of resistant populations.
In each of the situations described above, the
evolution of resistance was over a longer time frame,
ranging from an estimated 8 to 15 years of glyphosate
selection pressure. Recent efforts by Neve et al 54,55
provide an interesting perspective on the evolution
of glyphosate resistance in rigid ryegrass. Evolution
of glyphosate resistance was predicted to occur at
a relatively high rate (and estimated 90% of rigid
ryegrass populations) in a no-tillage environment.
When the complexity of the crop rotation was
increased, the evolution of resistance was not predicted
to occur. Other factors such as application timing,
Pest Manag Sci 61:301–311 (2005)
Herbicide-resistant crops and weed resistance to herbicides
inclusion of other herbicides and rotation of herbicides
also had a negative impact on the evolution of
glyphosate resistance.
2.2.4.2 Conyza canadensis
Unlike the time frame demonstrated by Lolium
spp, horseweed (C canadensis) evolved 8- to 13-fold
glyphosate resistance within 3 years of the adoption
of glyphosate-resistant soybean and the concomitant
use of glyphosate.40 However, some variation among
populations with regard to the level of resistance has
been observed.56 Tennessee horseweed populations
demonstrated a 4-fold increase in resistance compared
to the sensitive populations.56,57 This level of wholeplant resistance was also reported when the Delaware
populations were further evaluated.58 Horseweed, like
many other weeds that have evolved herbicide resistance, appears to have the ‘innate ability’ to evolve
resistance to herbicides with different mechanisms of
action.59 Anecdotal reports suggest that glyphosateresistant horseweed populations are now frequent in
the mid-Atlantic, Mid-south, Mississippi River Delta
and Mid-west regions of the USA, and represents
a serious problem in no-tillage cotton production.
Herbicide resistance in a weed like horseweed is the
worst-case scenario. Notably, horseweed is adapted
to conservation tillage agroecosystems, is essentially
autogamous but can cross-pollinate (<10%), and
produces many seeds that are wind-dispersed.60,61
Furthermore, recent research reports that the resistance trait in glyphosate-resistant horseweed is due to
an incompletely dominant single locus nuclear gene.58
Thus, the rapidity of the evolution of glyphosate resistance in horseweed and the large geographic distribution of these populations is understood. Furthermore,
the difficulty of managing horseweed with alternative
herbicides reinforces the fact that this is a significant
agronomic problem unless tillage is reintroduced into
the agroecosystem.
As with other glyphosate-resistant weeds, the
mechanistic basis of the resistance has not been easy to
identify, although a mechanism has been proposed.62
Differences in shikimate concentrations, comparing
resistant and sensitive biotypes, were noted, but both
biotypes were injured by glyphosate and accumulated
shikimate compared with the untreated controls.57,58
Injury was transitory in the treated resistant biotype
and shikimate concentrations declined 2–4 days after
treatment, thus indicative of resistance, while in the
sensitive biotype shikimate concentration continued
to increase. The implications of the differential
shikimate accumulation with regard to the resistance
mechanism were not definitive and several other
hypotheses to explain the resistance were offered.57
These ideas included numerous isoforms of EPSPS
(EC 2.5.1.19) in the plant, each with different
inhibition kinetics to glyphosate, the presence of
glyphosate oxidase reductase (GOX) resulting in the
metabolism of glyphosate over time, or an altered
EPSPS which would not allow competitive binding
Pest Manag Sci 61:301–311 (2005)
with glyphosate and the resultant inhibition of the
enzyme function. Differential retention, uptake and
metabolism were ruled out as possible mechanisms
of resistance in horseweed.62 However, a consistent
correlation of translocation differences comparing
the resistant and sensitive biotypes was observed
and suggested to be the mechanism of glyphosate
resistance in horseweed. The differential translocation
was attributed to differences in cellular distribution
and phloem loading resulting in reduced translocation
of the glyphosate and subsequent inhibition of
EPSPS.62 This explanation of glyphosate resistance
in horseweed is being investigated by a number of
research groups and further assessments will likely be
available in the near future.
2.2.4.3 Interspecific hybridization between Conyza
species
Interspecific hybridization between indigenous weedy
plants has been commonly reported and natural
hybridization in Conyza has been documented in
numerous instances.63 – 65 These hybrids do not typically evolve into significant weed problems. However,
the implication of hybridization between herbicideresistant and sensitive weed populations and the
introgression of the resistance trait is important.
Glyphosate-resistant horseweed has become a significant problem (see Section 2.2.4.2) and the potential
for interspecific hybridization with glyphosate susceptible dwarf fleabane (C ramosissima Cronq) was
determined in the greenhouse. Both weeds are native
to Iowa, although the dwarf fleabane is not known to
frequently infest croplands.66
The glyphosate-susceptible dwarf fleabane was
collected in Ames, IA, while the glyphosateresistant horseweed (C canadensis) was provided by
Mark VanGessel. Reciprocal crosses between ten
C canadensis × C ramosissima plant pairs (families)
generated the interspecific hybrid (FH
1 ), and hybrid
progeny (FH
2 ) populations were isolated by selfing
of the FH
1 in isolation. Transfer of the glyphosate
H
resistance gene in C canadensis to the FH
1 and F2
populations and to C ramosissima through backcrosses
was confirmed; the specific details of the morphological relation of the interspecific hybrid and the parent
Conyza can be found in two papers.58,67 The trait
for glyphosate resistance was dominant in the FH
1 and
FH
2 populations and introgressed whether the resistant
C canadensis parent served as pollen donor or pollen
receptor. Noteworthy, the relative level of glyphosate
resistance of the FH
1 was greater than that of the
resistant C canadensis parent (Fig 2). Furthermore,
resistance was conserved in the FH
2 at a level similar
to the original resistant parent. Research is currently
planned to assess the ability of the interspecific Conyza
hybrid to adapt to Iowa agroecosystems.
2.2.4.4 Amaranthus tuberculatus
Common waterhemp (Amaranthus tuberculatus) control in the Mid-west with glyphosate has been variable
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Visual injury (%)
100
C. ramosissima
C. canadensis
80
60
40
20
Visual injury (%)
0
100
Hybrid progeny
Interspecific hybrid
80
60
40
20
0
0.00 0.42 0.85 1.70 3.40 6.80 13.6
Glyphosate (kg AE
ha-1)
0.00 0.42 0.85 1.70 3.40 6.80 13.6
Glyphosate (kg AE ha-1)
Figure 2. Whole-plant rate response injury ratings of the dwarf fleabane (Conyza ramosissima), the resistant horseweed (Conyza canadensis), the
H
interspecific hybrid (FH
1 ), and hybrid progeny (F2 ) populations to glyphosate. Bars represent the mean of four replications and two experiments
(n = 8); extensions on bars designate 95% confidence limits associated with individual means.
with anecdotal reports of resistant populations. Most
of the management problems are attributable to the
inherent characteristics of this newly problematic
weed. These characteristics reflect variable dormancy
and requirements for germination, an extended germination period, high seed productivity and an apparent adaptation to conservation tillage programs.68,69
Furthermore, poor management decisions such as
reduced herbicide rates, delayed application timing
and poor application technique also contributed to the
widespread problems in controlling common waterhemp. However, there were a significant number of
complaints where the factors described above were
not considered to be in effect, and the likely cause
of the control issues was attributed to differential tolerance of the waterhemp populations to glyphosate.
The widespread adoption of glyphosate-resistant soybean was directly implicated in the development of the
waterhemp management issues.
The first investigated reports of control problems
were in 1998 from Badger and Everly, Iowa and
resulted in an assessment that portions of the common waterhemp population in those fields were not
responding to multiple applications of glyphosate,
while the majority of the population was sensitive.70,71
Reports from other Mid-west states corroborated
the findings from Iowa and suggested that common waterhemp plants survived glyphosate applied at
6.72 kg ha−1 and produced viable seed.72,73 In seedling
assays, Iowa populations demonstrated a GR50 of
306
0.3 to 0.8 mM glyphosate for the sensitive phenotype and 8.01 mM glyphosate for the putative resistant
phenotype.70 A divergent recurrent selection of the
phenotypes resulted in a 1.7- and 3.5-fold increase in
phenotypic divergence at the whole plant level, for the
first and second recurrent generations, respectively.71
Other observations noted differential shikimate accumulation with 5-fold less shikimate accumulating in
the resistant phenotype than in the sensitive phenotype, and a correlation between observed phytotoxicity
and shikimate accumulation.70,74 The specific mechanism(s) of glyphosate resistance in common waterhemp have yet to be determined.
2.2.4.5 Eleusine indica
Goosegrass (Eleusine indica (L) Gaertn) biotypes that
are confirmed to be resistant to glyphosate have
been identified in Malaysia.75 The population evolved
after an estimated 10 years of selection pressure
attributable to repeated applications of glyphosate, and
demonstrated a 2- to 4-fold resistance compared with
the sensitive biotypes. However, the plantation crops
in which the resistant goosegrass biotypes evolved
did not include any transgenic crops. Resistance
was the result of a less sensitive (5-fold) EPSPS
and ascribed to the substitution of proline at
position 106 for either serine or threonine.76,77 The
heritability of glyphosate resistance in goosegrass
was due to a single nuclear, incompletely dominant
gene that segregated in a 1:2:1 (S:I:R) ratio in
the F2 .78 At least one more glyphosate resistance
Pest Manag Sci 61:301–311 (2005)
Herbicide-resistant crops and weed resistance to herbicides
mechanism, in addition to target site modification,
was purported for goosegrass, stemming from research
concluding that some resistant populations possess
an EPSPS sequence identical to the susceptible
goosegrass population.79 These reports suggest that,
in goosegrass, glyphosate resistance is governed by at
least two independent mechanisms.
2.3 Naturally resistant species
A number of weeds have been described as having
inherent tolerance to various herbicides. Glyphosate
tolerance has been an important consideration for
many years, but was brought to prominence with
the adoption of glyphosate-resistant crops. An early
assessment suggesting that resistance to glyphosate
would not evolve was in error and also provided
some prediction of tolerant weed species.38 A
number of mechanisms by which weeds could be
tolerant to glyphosate were predicted and subsequent
reports and anecdotal observations validate the early
assessment.80 Differential absorption of glyphosate,
chemical composition of the epicuticular wax, leaf
angle and other mechanisms can account for tolerance
in various weed species.
2.3.1 Commelina communis
Recent grower reports suggest that Asiatic dayflower
(Commelina communis L) is becoming a serious weed
problem in isolated soybean, peanut and cotton
fields in the Mid-west, Mid-south and Southeast.
In glyphosate-resistant cotton, for example, Asiatic
dayflower in addition to pigweed (Amaranthus spp)
and morningglory (Ipomoea spp) are becoming more
difficult to control with glyphosate.81 The occurrence
of Asiatic dayflower is attributable to the adoption
of glyphosate-resistant crops and the concomitant
use of glyphosate as the primary or sole strategy for
weed control. Apparent natural tolerance to glyphosate
and other biological characteristics contribute to the
inability of growers to manage this weed effectively.82
Other herbicides used for weed control in soybean
do not demonstrate high levels of efficacy against
this weed. The best Asiatic dayflower control was
provided by three timely applications of glyphosate,
but sufficient escapes occurred, thus suggesting that
the weed would increase in future prominence.
2.3.2 Abutilon theophrasti
Velvetleaf (Abutilon theophrasti (L) Medic) has historically been described as difficult to control with
glyphosate.83,84 However, the tolerance of this economically important weed to glyphosate was not an
issue until the wide spread adoption of glyphosateresistant soybean. Recent reports suggest that the
survival of velvetleaf after exposure to glyphosate is
rate-dependent, but can be quite high.85 Velvetleaf
survival ranged from 46 to 81% with glyphosate
applied at 420 g AE ha−1 and dropped to 13 to 37%
at 840 g ha−1 . Plants were damaged and biomass
accumulation compared with untreated velvetleaf was
Pest Manag Sci 61:301–311 (2005)
reduced 90% by the high glyphosate treatment. However, injured plants did develop viable seed, thus
suggesting an increasing problem for future velvetleaf
management with glyphosate. The tolerance mechanism in velvetleaf was apparently associated to the
differential disruption of cellular processes in source
leaves and sink tissues, in addition to a mitigation of
water movement to the shoot, as consequence of inhibition of cellular processes in the root.86 Shoot and
root meristems in velvetleaf are particularly sensitive to
glyphosate compared to other tissues in the plant. This
is particularly the case when sublethal applications are
used, thus facilitating the differential translocation of
glyphosate to the meristems.87
2.3.3 Chenopodium album
Common lambsquarters (Chenopodium album L) is
adapted to conservation tillage systems and has
been a difficult weed to manage, irrespective of the
tactic used. Recent anecdotal observations in Iowa,
Minnesota and Wisconsin suggested that common
lambsquarters populations were not responding to
glyphosate in glyphosate-resistant soybean.
Lambsquarters, in addition to pigweeds (Amaranthus spp), copperleaf (Acalypha spp) and giant ragweed
(Ambrosia trifida L) have become prevalent species
in glyphosate-resistant soybean fields.81 Field investigations by the author resulted in an assessment
that poor management decisions, unfavorable weather
and other biologically controlled factors, rather than
differential tolerance to glyphosate, were the cause
of the inconsistent common lambsquarters control.
However, other observations (C Boerboom, pers
comm) suggested that, indeed, phenotypic differences
in tolerance were evolving in common lambsquarters. Recently, differential response to glyphosate was
reported in a common lambsquarters biotype from
Westmoreland County, Virginia.88 Compared to the
susceptible biotype from Montgomery County, Virginia, the Westmoreland biotype was less affected by
glyphosate at rates of 1.12 kg AE ha−1 . Notably, the
trait for glyphosate tolerance was apparently inherited
to the progeny, with some F2 plants demonstrating
visual injury of 68% at rates of 2.24 kg AE ha−1 . The
author suggests that this weed will continue to increase
in prominence and the use of transgenic crops will
exacerbate the problem.
2.3.4 Dicliptera chinensis
Chinese foldwing (Dicliptera chinensis (L) Juss) is a
member of the Acanthaceae and is indigenous to
East Asia and Taiwan. This plant has become a
serious weed problem in lowland orchards and is
described to be naturally resistant to glyphosate.89 The
resistance was attributed to higher EPSPS activity that
was further elevated by glyphosate. Increased EPSPS
mRNA and protein were observed 8 h after glyphosate
treatment and gene amplification was apparently not a
factor. Selection pressure from repeated glyphosate
applications in the orchards caused this plant to
307
MDK Owen, IA Zelaya
increase in prominence as a weed, but there was
no evidence that transgenic crops contributed to the
resistance.
2.4 Consequences of weed population shifts
The pervasive question that must be answered is
whether a weed population shift, whether attributable
to ‘ecological adaptation’, natural tolerance or evolved
resistance, is of economic importance. Herbicide
resistance is dispersed world-wide, weed species
adapted to current agroecosystems are reported,
and naturally resistant weed species appear to
be increasing.9,21,23,26 – 28 While weed population
shifts and the evolution of herbicide resistance are
inevitable consequences of the use of herbicideresistant crops and the adapted herbicide(s), the
relative economic importance will depend on the
specific agroecosystem.90 In the maize and soybean
agroecosystem prevalent in the Mid-west USA, the
economic risks, while not completely assessed, appear
to be less than anticipated. Regardless, it is important
to appraise the situation and make appropriate
adjustments in weed management tactics to keep
weed shifts and the evolution of herbicide resistance
from becoming an economic problem, whether or
not herbicide-resistant crops are a component of the
agroecosystem.9
3 HERBICIDE-RESISTANT CROPS AS WEEDS
Maize and soybean have consistently been volunteer
weeds in production systems where maize and soybean are rotated. However, very little information is
available that describes the management or economic
importance of the problem. Growers generally do not
see volunteer maize or soybean as a serious problem
and, historically, acceptable management tactics exist.
However, with transgenic traits for herbicide resistance, management of volunteer maize and soybean
could become more costly. The author suggests that
this may indeed be the case in most agroecosystems
in which maize and soybean are grown. Furthermore,
the occurrence of volunteer maize in soybean grown
in rotation could potentially increase maize insect or
diseases by allowing populations to increase during the
year soybean was grown. The biggest potential impact
would be where the herbicide resistance trait was the
same in the rotational crops (eg glyphosate-resistant
maize as a volunteer weed in glyphosate-resistant
soybean). However, if the herbicide-resistant maize
volunteers into a conventional cultivar soybean, or
if the transgene is for resistance to insects or plant
pathogens, the volunteer maize would not have a significant impact on the management tactics.
3.1 Maize (Zea mays L)
Factors that influence the likelihood of volunteer
maize becoming established as a weed include
pest infestations, harvesting and tillage. Insect
and disease infestations increase the potential for
308
pre-harvest maize ear losses, resulting in more
volunteers the following year. Maize losses during
harvesting occur directly by gather losses (grain is
missed or dropped by the harvest machinery) and
cylinder and separator losses which reflect the efficiency of grain shelling by the harvest machinery.91
Volunteer maize problems are a greater concern in
conservation tillage systems where seeds remain on or
near the soil surface. Management of volunteer maize
has not been a major concern in soybean. Graminicides (eg diclofop) or glyphosate, applied selectively,
have been very effective management tactics.92 Currently, in soybean, glyphosate is used to manage all
weed problems including volunteer maize. However,
with the increased adoption of glyphosate-resistant
maize hybrids, growers in the Mid-western USA are
experiencing problems managing volunteer maize with
glyphosate, even if glyphosate-resistant maize was not
planted the year previous to the glyphosate-resistant
soybean. The glyphosate resistance transgene has
moved widely in pollen and has resulted in volunteer maize with glyphosate resistance. As a result of
the transgene pollen movement, growers now often
include graminicides to control the weed problem. It
was estimated that with a favorable wind direction for
cross-pollination to occur and a plot distance of 30 m,
2% of the non-transgenic maize contained the transgene for glyphosate resistance.93 Another potential
problem is the contamination of seed fields, resulting
in contaminated seed lots.
Models that predict the potential for pollen
movement have been developed, but there are
limitations on the accuracy of the prediction.94,95
The simplicity of current models limits the ability
to predict the amount of pollen that can move
further than 250 m, and to assess the impact of
climactic conditions. The maximum distance for
cross-pollination was measured to be 200 m from the
pollen source.96 In other studies, only 0.5–0.75% of
viable maize pollen was estimated to move 500 m from
the source plant.97 However, the occurrence of pollen
does not mean that transgenic trait movement occurs
over great distances. Furthermore the occurrence of
transgenic pollen in a non-transgenic maize field does
not mean pollination was successful.97 Increasing
isolation distance between transgenic maize and nontransgenic maize is a useful tool in containing gene
flow.96 However, distances necessary to maintain a
near 0% transgenic contamination are too large to
be realistic.98 Research recently conducted at Iowa
State University demonstrated clearly that distances
approaching 500 m were not sufficient to keep
transgene movement in maize contained.99 Thus,
the importance of herbicide resistance in volunteer
maize is likely to become an increasing problem as the
adoption of glyphosate-resistant hybrids increases.
3.2 Soybean (Glycine max L)
Soybean frequently occurs as a volunteer weed
problem in rotation crops but is not generally
Pest Manag Sci 61:301–311 (2005)
Herbicide-resistant crops and weed resistance to herbicides
considered difficult to manage. Thus, there is no
literature on the topic. Soybean seeds that are
lost during harvest do not over-winter well, and if
volunteer plants develop in the rotational crop, losses
attributable to interference are minimal. Furthermore,
soybean are essentially autogamous, so that transgene
movements via outcrossing attributable to pollen
movement are negligible. In soybean/maize rotations,
herbicides typically used for weed control in maize
(eg atrazine) effectively control volunteer soybean.
However, in glyphosate-resistant maize, volunteer
glyphosate-resistant soybean would be difficult to
control with only glyphosate.
4 CONCLUSIONS
The adoption of herbicide-resistant crops will continue. Adoption in major crops such as soybean, cotton
and canola is perceived to have slowed, but the majority of hectares planted are already herbicide-resistant
cultivars. The adoption of glyphosate-resistant maize
will increase, albeit more slowly than experienced in
soybean. The relative slow adoption of this transgenic
trait reflects a number of issues, but concerns about
market acceptance are important. Regardless, growers
perceive that the benefits of the herbicide resistance
characteristic outweigh the risks. It is clear that the
widespread adoption of herbicide-resistant cultivars,
particularly glyphosate-resistant crops, has dramatically impacted weed communities. Weed population
shifts to naturally resistant species, species with inherent biological characteristics that make the populations
difficult to manage (eg delayed emergence), and the
evolution of herbicide-resistant biotypes are real, as
are the immediate economic issues attributable to the
adoption of herbicide-resistant crops and the concomitant use of the herbicide. The speed at which
these changes have occurred has caused significant
concern. However, given the level of selection pressure that these crop production systems impart on the
agroecosystem, it is not surprising that the changes
in the weed communities have occurred as rapidly
as demonstrated. These trends, weed shifts, tolerance
and evolved resistance, are not predicted to slow in
the immediate future.
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