ISIS Report 03/03/10
Glyphosate Resistance in Weeds
The Transgenic Treadmill
Glyphosate resistant weeds may spell the end of patented herbicide
tolerant crops, but can farmers exit the transgenic treadmill that’s very
profitable for Monsanto? Prof. Joe Cummins
An evolving problem
Glyphosate herbicide was patented and sold by Monsanto corporation
since 1974 under the trade name and proprietary formulation Roundup. The
herbicide has been used widely in agriculture, forestry, aquaculture, alongside
roads and highways, and in home gardening. Glyphosate is a broad-spectrum
herbicide that poisons many plant species so it is frequently used to ‘burn
down’ weeds on a field prior to the planting or emergence of crops.
Before 1996, weeds were not observed to have evolved
resistance to glyphosate in the field, but since then, the introduction of
transgenic glyphosate tolerant crops has led to evolution of a number of resistant
weeds as the result of the greatly increased use of the herbicide particularly during
the post-emergent growth of the crops. Glyphosate reisistant 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 agro ecosystems as are populations of
horseweed (Conyza canadensis (L) Cronq) .
In regions of the USA where transgenic
glyphosate resistant crops dominate, there are now evolved glyphosate-resistant
populations of the economically damaging weed species Ambrosia
artemissifolia (rag weed), Ambrosia trifida L.(great ragweed), palmer
pigweed (Amaranthus palmeri), common water hemp (Amaranthus rudis)
, rough fruit amaranth (Amaranthus tuberculatus) and various Conyza
(horse weed ) and Lolium (rye grass) species.
Likewise, in areas of transgenic glyphosate resistant
crops in Argentina and Brazil, there are now evolved glyphosate resistant
populations of Johnson grass (Sorghum halepense) and Mexican fireplant (Euphorbia
heterophylla) . These herbicide resistant weeds pose a clear threat to the
transgenic crops dominating North and South America .
Can resistance be managed?
There is no simple remedy for the evolution of resistance to
glyphosate. Interestingly, the inventor of both glyphosate and the herbicide
tolerant crops, Monsanto Corporation, does not appear to be engaged in finding
remedies for the invasion of resistant weeds. There has been an effort to
remedy the invasion of resistant weeds by the academic community. Simulation
modeling has been developed. Glyphosate use for weed control prior to crop
emergence is associated with low risks of resistance. These models are based on
assumptions that low risks can be further reduced by applying glyphosate in
sequence with other broad-spectrum herbicides prior to crop seeding . Post-emergence
glyphosate use, however, associated with glyphosate-tolerant crops, very
significantly increases the risks of resistance evolution. Annual rotation with
conventional crops reduces these risks, but the proportion of resistant
populations can only be reduced to close to zero by mixing two of three
post-emergence glyphosate applications with herbicides that have alternative
modes of action. Weed species that are prolific seed producers with high seed
bank turnover rates are most at risk of glyphosate resistance evolution. The
model is especially sensitive to the initial frequency of resistance alleles,
and other genetic and reproductive parameters, including weed breeding
system, dominance of the resistance trait and relative
fitness, influence rates of resistance. (Although these assumptions may be
quite irrelevant in view of numerous physiological mechanisms of the ‘fluid
genome’ that can produce resistant mutations in plants exposed to non-lethal
levels of glyphosate, as discussed in  (GM Crops Facing
Meltdown in the USA, SiS 46).
Over the past decade, the most problematic weeds
in agronomic cropping systems have shifted away from perennial grass and
perennial broad leaf weeds to primarily annual broadleaf weeds, although the
glyphosate resistance mechanisms in weeds are currently poorly understood .
It appears that post-emergent use of glyphosate may be a main contributor to
evolved glyphosate resistance, but eliminating post-emergent herbicide
treatment practically eliminates all the advantages of and hence the need for
herbicide tolerant crops.
Evaluation of herbicide programs for the
management of glyphosate-resistant waterhemp (Amaranthus rudis) in maize
involved pre-emmergent application with the herbicide glufosinate followed by a
post-emmergent treatment of the transgenic maize with glyphosate which
controlled water hemp better than pre and post emmergent treatment with
glyphosate alone .
Maize growing in the EU27 increased to over 13
million ha in 2007, most of which (>80 percent) grown in just eight
countries (France, Romania, Germany, Hungary, Italy, Poland, Spain and Bulgaria). The number of herbicides used to control the wide spectrum of weeds occurring
in all these countries is likely to decline in the future, and care need to be
taken to manage potential weed shifts to more difficult-to-control species and
to reduce the risk of selection for glyphosate-resistant weeds .
In 2002, a glyphosate resistant Johnson grass (Sorghum
halepense) appeared in Argentina and now covers at least 10 000 ha. The
introduction of novel genetically modified crops promoted the use of more
herbicides. This in turn reinforces the emergence of herbicide-resistant weeds,
constituting a new phenomenon of intensification, the “transgenic
Many herbicide tolerant crops become “volunteer”
weeds that infest crop rotations. Those weeds complicate cultivation,
contaminate crops, and enhance gene transfer to weedy relatives. A transgenically
mitigated (TM), dwarf, herbicide-resistant construct using a gibberellic
acid-insensitive (Deltagai) gene in the B. napus crop was effective in
offsetting the risks of transgene establishment in volunteer populations of B.
napus (oilseed rape) . Dwarfing the transgenic crop did not hurt yield
of the oil seeds, but controlled the volunteer weeds because they were shaded
by a taller crop. Mitigation by dwarfism worked well in greenhouse experiments
but failed in field experiments. The proposed mitigation increased escape and
persistence of transgenic weeds . An alternative mitigation strategy for
transgenic rice involved the introduction of a potpourri of traits including
dwarfism, non-shattering, no secondary dormancy and herbicide sensitivity .
The companies selling herbicides and herbicide
tolerant transgenic crops are in no hurry to control herbicide resistant weeds;
for them, the multiple herbicides used to control transgenic weeds may come as
an economic blessing. It is the farmers and the rest of society that suffer.
basis of glyphosate tolerance
kills plants by interfering with the synthesis of the amino acids
phenylalanine, tyrosine and tryptophan. It does this by inhibiting the enzyme
5-enolpyruvylshikimate-3-phosphate synthase (EPSPS), which catalyzes the
reaction of shikimate-3-phosphate (S3P) and phosphoenol pyruvate to form
5-enolpyruvyl-shikimate-3-phosphate (ESP). ESP is subsequently dephosphorylated
to chorismate, an essential precursor in plants for the aromatic amino acids:
phenylalanine, tyrosine and tryptophan. These amino acids are used as building
blocks in peptides, and to produce secondary metabolites such as folates,
ubiquinones and naphthoquinone. X-ray crystallographic studies of glyphosate and
EPSPS show that glyphosate functions by occupying the binding site for phosphoenol
Some micro-organisms have a version of
5-enolpyruvoyl-shikimate-3-phosphate synthetase (EPSPS) that is resistant to
glyphosate inhibition. The version used in genetically modified crops was
isolated from Agrobacterium strain CP4 (CP4 EPSPS) that was resistant to
glyphosate. The CP4 EPSPS gene was engineered for plant expression by fusing
the 5' end of the gene to a chloroplast transit peptide derived from the petunia
EPSPS. This transit peptide was used because it had shown previously an ability
to deliver bacterial EPSPS to the chloroplasts of other plants The chloroplasts
of higher plants synthesize amino acids phenylalanine, tyrosine and tryptophan .
The genetic basis of many of the glyphosate
resistant weeds remains unknown; but those studied in detail show that there
is no single genetic alteration responsible in all of the resistant weeds.
Some populations of goosegrass from Malaysia, rigid ryegrass from Australia,and Italian ryegrass from Chile exhibit target site-based resistance to glyphosate through
changes at amino acid 106 of the 5-enolpyruvylshikimate-3-phosphate synthase
(EPSPS) gene. Mutations change amino acid 106 from proline to either serine or
threonine, resulting in an EPSPS weakly resistant to glyphosate. The moderate
level of resistance is sufficient for commercial failure of the herbicide to
control these plants in the field. Other mechanisms of resistance include a
nontarget site resistance mechanism has been documented in glyphosate-resistant
populations of horseweed and rigid ryegrass from the United States and Australia, respectively. In these resistant plants, there is reduced translocation of
glyphosate to meristematic tissues. Both of these mechanisms are inherited as a
single, nuclear gene trait .
EHSPS gene amplification has been found to lead
to glyphosate resistance in Amaranthus palmeri populations from Georgia, in comparison with normally sensitive populations. EPSPS enzyme activity from
resistant and susceptible plants was equally inhibited by glyphosate. Genomes
of resistant plants contained from 5-fold to more than160-fold more copies of
the EPSPS gene than did genomes of susceptible plants. Quantitative RT-PCR on
cDNA revealed that EPSPS expression was positively correlated with genomic
EPSPS relative copy number. The amplified genes were not clustered on the
chromosomes but distributed among all of the chromosomes [15, 16]. These
results suggest that the EPSPS genes were amplified through mobile genetic
elements (jumping genes). Interestingly, in a laboratory experiment with
alfalfa cells in culture reported eight years before the Amaranthus
investigation gradual stepwise increases in glyphosate in culture medium led
to gene amplification of the EPSPS gene ‘
. Another evolutionary glyphosate resistance mechanism was
observed in the horse weed. The mutant weeds rapidly pumped the herbicide into
vacuoles preventing contact of the herbicide with the chloroplast .
The evolution of glyphosate resistance among weeds that interfere
with the productivity of crops is approaching catastrophic proportions. The
evolutionary process leading to the resistant weeds has been described as a
“transgenic treadmill” that renders current use of transgenic crops unsustainable.
As current transgenic crops are rendered obsolete through weed resistance, the
crops will be replaced with new transgenic varieties made available at higher
prices to the farmers  (GM Crops Increase
Herbicide Use in the United States , SiS 45) followed by another
round of weed evolution to resistance. The only escape from this treadmill is
to shift comprehensively to organic agriculture , as farmers have discovered
in India  (Farmer Suicides
and Bt Cotton Nightmare Unfolding in India, SiS 45).
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There are 4 comments on this article so far. Add your comment
|Tim Croughan Comment left 6th October 2010 09:09:32|
I think this article is excellent. For me it was also interesting to learn that Jack Widholm, who is really a great guy, did such ground-breaking work on this topic (ref. 17).
|Rory Short Comment left 3rd March 2010 17:05:06|
In my understanding herbicides and the subsequent development of genetic modifications in crop plants in order to render them herbicide resistant are both the natural consequence of viewing Nature as wholly separate from ourselves.
This view is completely erroneous. We are part of Nature.
A natural by product of this erroneous view is an exploitative as opposed to a cooperative approach toward Nature. I think the likes of companies such as Monsanto and their corporate behaviours exemplify this erroneous view.
|MICHEL LE CHAPELLIER Comment left 22nd February 2011 11:11:49|
I was looking for a document related to evolving risks that could be read by my students.
This one is interesting and short. Furthermore, it shows how references may be used.
|Solomon Adejoro Comment left 28th July 2012 19:07:53|
I am a researcher in the fields of Weed and Soil Science. I stumbled upon this article and found it so educating that I can't discard it. I have saved the article because it is going to be a useful reference material in my research work. Kindly forward future articles of this publication to my Email address provided herewith. Many thanks.