Lakhasly

HERBICIDE TOLERANCE IN PLANTS
Homer M. LeBaron
President, Weed Science Society of America
Senior Research Fellow, New Technology and
Basic Research, CIBA-GEIGY Corporation
Herbicide Resistance in Plants1
The first discovery of a triazine-resistant weed (common ground-
sel) was in western Washington in the late 1960s. The subsequent
widespread and frequent occurrence of other triazine-resistant weeds
over the past 20 years have made triazine herbicide-resistance the best
known and most studied case of herbicide-resistance. Triazine-resis-
tance has also been of great interest because of the importance and ex-
tensive use of this group of herbicides. If other single target site residu-
al herbicides (e.g., diuron) were used as extensively and continuously
as the triazines, they would have almost certainly led to resistant bio-
types.
Although weeds have taken longer to evolve herbicide-resistance
compared to insect pests and pathogens, biotypes of 40 broadleaves
and 15 grass weed species are known to have developed resistance to
triazine herbicides somewhere in the world. A total of 45 weed bio-
types (29 broadleaves and 16 grasses) have evolved resistance to 14
other types of classes of herbicides, making a grand total of 100
herbicide-resistant weed biotypes to date. Only 21 of the triazine-re-
sistant biotypes and 16 biotypes resistant to other herbicides have
been found in the U.S., but one or more of these resistant biotypes
have invaded 39 states, six provinces of Canada and 27 other countries.
’LeBaron noted that this paper was represented as the President of the
Weed Science Society of American and as a weed scientist, rather than
a representative of CIBA-GEIGY Corporation.
Past experience has shown that weeds resistant to triazines can be
managed or restrained within a reasonable limit. In the U S. the total
area of land or crops infested with triazine-resistant weeds is still rela-
tively limited (estimated to be about 3,000,000 acres) and does not
seem to be expanding rapidly, except in a few states where continuous
corn or no-tillage farming is being practiced or good alternative herbi-
cides are not used. In most areas of the U.S. where triazine-resitant
weeds have evolved it has not even been necessary or desirable to cease
using the triazine herbicide of choice, due to the many susceptible
weeds that are still usually prevalent. In a few cases, the resistant bio-
types have even disappeared.
It is very important for nonbiologists to understand that an essen-
tial requirement of herbicides is that they control all weeds through-
out the season. This may be from 5 to 25 species, not just the one or
two pests that insecticides and fungicides usually try to control. If all
but one species is controlled, little has been accomplished because that
species will take over. This also makes it difficult for weed scientists to
deal with weed thresholds because if the “escapes” are resistant to the
herbicide used, within one or two years the field will likely be a solid
stand of resistant weeds. Even if they are susceptible escapes, many
weeds tend to expand to fill up the space available, which again is dif-
ferent from insect and disease pests. Most herbicides must also have
some soil persistence in order to control weeds that germinate later in
the season.
Over the 45 years that modern herbicides have been developed and
used extensively, there have been many cases of differential tolerance
within various weed species, such as intraspecific resistance to 2, 4-D,
Dalapon®, and other herbicides. There are seen many examples of evo-
lution toward interspecific herbicide tolerance. Researchers who have
been trying to control weeds for some time have learned in many ways
that nature is neither an exact nor fixed science. Nothing remains con-
stant and weeds have been around a lot longer than scientists have.
Weeds have learned to adapt and evolve to survive.
Some of the modern chemical tools have been so spectacular com-
pared to the cultivator and hoe that we have become accustomed to
seeing clean, weed-free fields, and become a bit complacent. Even
when triazine resistance evolved, an easy way to circumvent these
interlopers was found, with a new generation of spectacular herbicides
Herbicide Resistance in Plants
(e.g., sulfonylureas, imidazilinones) which are effective at grams per
acre instead of pounds per acre. They are just what was needed to help
solve environmental concerns and other problems while adding dimen-
sion and flexibility to our weed control technology. Again weed scien-
tists marveled at the success and potential of their inventions, but did
not look back to see what nature was doing. Within the past few years,
an increasing number of weeds have evolved resistance to these and
several other new types of herbicides.
NEW ROLE OF HERBICIDE-RESISTANT CROPS
Knowledge about herbicide sites and modes of action has been essen-
tial in the research and understanding of herbicide-resistance mecha-
nisms. Herbicide-resistant weeds have also been valuable scientific
tools, contributing greatly to the understanding of herbicide modes of
action, plant biochemical and physiological processes, molecular gene-
tics, physical structure, and anatomy. However, it is interesting and
significant that the mechanisms of resistance developed by weeds are
often different from the mechanisms of selectivity to those herbicides
in most crops. This is certainly true with the most prevalent and tho-
roughly studied cases of herbicide-resistance, including the triazines,
dinitroanilines, and acetolactate synthetase (ALS) inhibitors.
For example, in the goosegrass (Eleusine indica), weed biotyped re-
sistance to trifluralin, the tubulin in the roots, is apparently altered so
that dinitroaniline herbicides are not effective in preventing tubulin
polymerization into microtubules, which is assumed to be the mecha-
nism of action of these herbicides. However, selectivity in most crops
to these herbicides is believed to be due to the ability of their tap roots
to rapidly grow through the treated soil layer or differential lipid con-
tent in seeds, thereby avoiding significant herbicide exposure.
Resistance mechanisms in weed biotypes to ALS inhibitors are ap-
parently due to an alteration in the gene coding for acetolactate syn-
thetase, resulting in various forms of insensitive ALS enzymes, the
main target site of these herbicides. Crop tolerance, however, seems to
be mostly dependent on differential metabolism.
Research to date indicates that most of the triazine-resistant bio-
types lack the normal triazine binding sites in their chloroplasts,
whereas crop selectivity is due mainly to metabolism or translocation
differences. Triazine-resistant velvetleaf (Abutilon theophrastis) in
Maryland is an exception in that resistance is due to enhanced glu-
tathione transferase activity.
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While most crops and weeds are susceptible to paraquat,
paraquat-resistant horseweed (Conyza) biotypes may be insensitive
to the herbicide due to elevated levels of superoxide dismutase and
other enzymes, or to differential binding or distribution of the
herbicide in the weed.
Recent research on the physiological basis of mecoprop resistance in
chickweed indicated that resistance is due to reduced mecoprop bin-
ding at the sites of action in resistant plants. Data on mechanisms of
most other types of herbicide-resistance in weeds are still not com-
plete.
RESISTANT WEEDS AND CROPS AND THE FUTURE OF HERBICIDES
Resistance to the ALS inhibitors and other newer herbicides has al-
ready become a very serious issue. Industry, especially Du Pont, has
responded quickly and appropriately to completely modify their mar-
keting strategy and research programs to manage potential weed resis-
tance to their sulfonylureas. Such responsible reaction of the part of
the industry must be encouraged and supported. Everyone connected
with agriculture should view herbicides as important nonexpendable
tools that must be preserved for future generations. It is gratifying to
hear and see more about product stewardship than ever in the past.
Past performance in pest resistance management and use of our insect-
icides and fungicides, both in industry and on the farm, has often been
irresponsible and shameful, and has contributed much to a poor public
image. There must be better in management of herbicides and resistant
weeds.
Of special concern is the occurrence of cross-resistance to many
herbicides within the same species. The few cases to date are still a
long distance away. The most noted examples are Lolium rigidum (an-
nual ryegrass) in Australia and Alopecurus (blackgrass) in the U.K.
However, it is very worrisome that multiple cross-resistance to her-
bicides can occur in plants, apparently by similar mechanisms (meta-
bolic detoxification, e.g., mixed function oxidases) to some insects
which rapidly evolve resistance to insecticides. Such efficient oxida-
tion of foreign organic chemicals may prevent almost any herbicide
from reaching the target site intact. When I first saw the one known
case of diclofop methyl resistant ryegrass in Australia about three and
a half years ago, and I learned that it was cross-resistant to most sul-
fonylureas, I warned them that they were potentially facing the worst
Herbicide Resistance in Plants
case of herbicide-resistance I knew of in the entire world. This has
proven to be the case, as this multiple-resistant weed has become
widespread throughout most of the cereal producing areas of Austra-
lia. The solutions to this problem will not be easy, and cultural and ag-
ronomic methods will have to be included as well as, or possibly in
place of chemical methods. Because of the striking ability this weed
has for developing resistance to many herbicides, not only in Australia
but in other parts of the world, Lolium is the housefly or Colorado pota-
to beetle of the plant kingdom. A diclofop methyl-resistant Lolium mul-
tiflorum (Italian ryegrass) was recently discovered in Oregon. It was
found to have some degree of cross-resistance. This genus must be re-
spected, and we must avoid in any way possible evolving such plants
with multiple resistant potential.
Because of much lower application rates, with less perceived hu-
man, animal and environmental exposure and risks, a very strong per-
ception exists among government agencies and policymakers that the
new sulfonylurea herbicides will replace many of those in current use.
This perception comes at a time when some of the earlier herbicides
are being discontinued or are in trouble because of economics, reregis-
tration requirements, toxicology and environmental concerns. There
will be a great need for the older herbicides and other tools of agricul-
tural technology in the future. Chemical herbicides must be a major
part of the agricultural technology in the decades ahead to provide the
constantly greater demand for food, fiber and shelter, with greater cost
effectiveness. But other means of pest control must not be discarded,
nor should there be too much dependence on chemicals alone. Herbi-
cide-resistance is acting as a self-imposed limiting system of nature,
and nature sets the rules—be flexible or lose.
With the first invasion of resistant weeds, prompt action is essen-
tial in order to avoid serious and more permanent problems. Preventive
action to avoid herbicide-resistant weeds from developing in the first
place is definitely the best strategy. It is virtually essential in all cases
of herbicide-resistance to have other classes or types of herbicides,
with alternate sites and mode of action, available. In some countries
and situations, control of triazine-resistant weeds has not been suc-
cessful, resulting in rapid invasion and almost total loss of these herbi-
cides in the area.
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I have great concerns and doubts whether we can be as successful in
avoiding or managing the more recent resistant biotypes as we have
been with triazine-resistant weeds in the past. Not only are herbicide-
resistant weeds appearing after fewer repeat annual applications of
some of the newer herbicides, but there seems to be me species that
have potential for resistance. It is likely that many, if not all, weeds
possess some ability to evolve resistance to these herbicides. In addi-
tion, the resistant biotypes are apparently equally fit and competitive
once they evolve, unlike most biotypes resistant to triazine herbicides.
Both wisdom and understanding developed on pest resistance to
pesticides must be utilized, as well as greater marketing control and
self-restraint than has thus far been demonstrated in U.S. agriculture,
must be exercised in order to protect or prolong the use of the sulfony-
lurea and other herbicides with a single site of action and high risk for
resistance. The following changes or strategy rules will be required:
—These herbicides should be marketed only in combinations, espe-
cially in major crops, if other types of herbicides are available as suit-
able partners.
—Crop and herbicide rotations should be used whenever possible. In
rotations, avoid those with the same weed spectra.
—Use of long residual ALS herbicides should be avoided or minimized.
—Use the lowest rates possible.
—Minimize the number of applications per season, and use only every
two or three years.
—Education and cooperation of industry management, marketing,
sales, extension, farmers, and others is essential.
—Government agencies and policymakers must realize that all possi-
ble herbicides must be retained as potential mixing partners.
— Industry should not develop and market ALS resistant crops or
crops resistant to only one herbicide with a high risk for resistance for
the purpose of greatly expanding their use. This approach should be
used to enhance tolerance in crop varieties, to avoid carry- over injury,
for specific and limited special problems, and for minor acreage and
high value crops. A major objective of developing herbicide-resistant
crops should be to provide more flexibility in control of resistant
weeds.
Herbicide Resistance in Plants
—These herbicides should be used in crops only where several other
good mixing partners, cultivation, and other weed control options are
available.
—Cultivators or other mechanical weed control options should remain
available. Conservation tillage systems may not be a long-term or con-
tinuing option.
—If possible, industry should continue to develop chemicals in this
class that will inhibit all types of ALS enzymes and overcome this re-
sistance.
—Develop other herbicides that do not have a single site of action and
are not as likely to induce resistance.
—Lastly, do not throw away the hoe, but rogue out the weeds that es-
cape if resistance occurs or is suspected, or use systems that preferen-
tially control resistant weeds.
Many politicians and those who like to tell farmers how to farm
mention that herbicide-resistant weeds are one more reason for aban-
doning herbicides in favor of other methods. This is fine if other me-
thods are actually available, profitable and environmentally desirable.
But resistant weeds require that all possible herbicides be retained so
that farmers have all possible options. Nature plays no favorites.
Weeds, as with insects and diseases, will tend to survive and evolve
resistance to any method used to control them.
I can agree with proponents of sustainable agriculture that we have
at times depended on herbicides too much, or have expected too much
from them. However, we should not ask farmers to get by without her-
bicides, and no one who likes to eat should try to compel them to do so.
Rather, we must learn to better manage herbicides and preserve them
by learning to use them as essential tools while avoiding and managing
resistant weeds. We must also make further scientific breakthroughs
or improvements in formulations, application technology, and han-
dling methods to reduce human and environmental exposure and risk.
These new low-rate herbicides must continue to be an important part
of our future defense against weeds.
There is no way that biological and other nonchemical methods of
weed control will totally replace chemicals in our lifetime. If anything
has been learned in the past 40 years, it is that we will need all the help
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we can get to keep ahead of the pests, and to depend on only one tool or
method against major pests is a sure road to failure and scientific
heresy. Chemicals will continue to be essential and the main line of
defense against weeds, and will help to produce the crops and pay for
the research on biological controls, biotechnology, and sustainable ag-
riculture while other tools are being developed.
As implied above, genetic engineers should reevaluate their strategy
in developing herbicide-resistant crops. Five years ago, there were over
100 scientists or laboratories working on triazine resistant crops. This
interest has greatly decreased for a number of valid reasons. The shift
in priority has been toward ALS inhibitors and glyphosate. To scien-
tists who are working on such a project for the purpose of using one of
these specific herbicides exclusively and continuously, I strongly re-
commend that you drop the effort. Not only will it take longer to get
the crop ready and approved for commercial introduction than origi-
nally planned, and resistant weeds may have already invaded your
market, but if your herbicide of choice is used repeatedly, it will likely
be only a few years before it will have resistance problems.
On the other hand, scientists should continue developing herbi-
cide-resistant crops with the objective of offering growers greater
weed control options and flexibility in the types of herbicides that can
be used, especially as a strategy to control herbicide-resistant weeds.
This research effort could also be justified by enhancing the natural
selectivity of the target crop or reducing potential carry-over injury to
rotational crops.
Most biotechnologists justified the need for genetically engineered
crops as a way to get rid of pesticides. Now with the same kind of regis-
tration requirements and scrutiny that chemicals have always been
subjected to required, biotechnologists are appalled at the confronta-
tions and opposition. We need to be honest with each other and recog-
nize that not only are biotechnologists working with live organisms
that can reproduce, but in most cases, they are considering replacing a
chemical with a chemical. While there may be some benefits of plant
development, confinement of the toxicants, human or environmental
risk, etc. there could even be more hazard from natural pesticides in
engineered plants versus those treated with synthetic chemicals, un-
less they do not remain in the edible part of the crop and the plant resi-
due is handled as a hazardous waste. But my major concern is that the
Herbicide Resistance in Plants
farmer needs all the help and options available, and we should not con-
sider that biotechnology and biocontrol are in competition or conflict
with chemicals, nor immune from resistance. It may be that pests can
soon evolve resistance to the “natural” chemical or method, as well as
those externally applied.
HERBICIDES AND LISA
Herbicides have already made great contributions to low input and
sustainable agriculture. The Low Input Sustainable Agriculture (LISA)
philosophy promotes conservation tillage, as do all weed scientists.
However, without herbicides, there would be little or no conservation
tillage in most crops. Soil conservation programs, agricultural sustain-
ability and production efficiency are, and will continue to be, abso-
lutely dependent upon herbicides. This does not mean that mechanical
(e.g., tillage, moving), biological (e.g., mycoherbicides, allelopathy,
cover crops), and other tools are of no value. However, these methods
will continue over the next 20 to 30 years, at least, to be very limited
in application, even though their development and use needs encour-
agement wherever they fit the problem. There are many ways that
herbicides can and are being used to protect and enhance the environ-
ment for use by humans, birds and animals, and in most cases, they
will be safer and have less environmental impact than other weed con-
trol tools such as mechanical tillage, biological (live organism) con-
trols, etc.
The switch from the moldboard plow and cultivator to conserva-
tion tillage systems makes us more dependent on herbicides, but the
benefits more than compensate for the risks. This trend should be con-
tinued and increased where it can be advantageous to agriculture, as
well as the environment. Conservation tillage not only protects 50 to
90 percent of essential topsoil that would otherwise be permanently
lost by water and wind erosion, but it prevents much more than just
inert soil moving into streams, rivers, lakes and air. This reduced ero-
sion, combined with the erodable cropland that has been planted to
grasslands or woodlands have already saved more than half a billion
tons per year of top soil. Much more soil will be preserved if the pro-
jected 40 million acres (11 percent of total cropland) is set aside over
the next two years and better herbicide programs could be developed
to make farmers more confident that the weeds can be controlled with-
out tillage. Some watershed studies in recent years have shown a rever-
sal from major losses to net gain in soil. The Environmental Protection
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Agency (EPA) and the public are increasingly concerned about pesti-
cides in groundwater since analytical advances have allowed us to mea-
sure very low and often meaningless levels of synthetic chemicals in
water, mostly traceable to point-source contamination. Virtually no-
thing is known about natural pollutants or mutagens that have been
and may still be in drinking water. Some scientists need to study the
effects of herbicides versus tillage practices on the movement of natu-
ral toxins (e.g., organics, inorganics, and microorganisms) into our
water and air, including their potential mutagenic or health effects,
identification, characterization, and quantification. Herbicides have
had beneficial effects on water quality through conservation tillage;
the whole picture needs to be seen.
Furthermore, it must not be assumed that LISA or alternate farming
methods have no environmental impacts. They may, in fact, cause
exposure to more toxic or objectional contaminants than do herbi-
cides. For example, I would prefer to drink water coming off of or from
under a field treated with herbicides and commercial fertilizers rather
than a field treated with 10 to 20 tons per acre of cow manure. We do
not know everything that manure contains, and it may be that very
little of it reaches groundwater, but there could be contaminants in
runoff water. We need to know what the effects and comparative risks
are, and not assume that LISA is a safer way to farm than using syn-
thetic chemicals. There is not, never has been, and never will be zero-
risk agriculture or life.
Another concern about LISA, or any arbitrary reduction in the use
of herbicides, is the phenomenon of biological changes with time. In
many situations, the weed populations and pressure are not the same
as 30 years ago. Where herbicides have been extensively used, some
species have almost disappeared and the weed seed density in the soil is
often much reduced. This is not obvious or easy to measure, especially
to nonbiologists, because there are still many weed seedlings that ger-
minate each spring. This phenomenon is even contributing to some of
the short-term successes from cutting back on herbicides. But, the full
effect of reducing or eliminating herbicides will not be seen the first
year. Nature will adapt and take advantage of any nitch available, and
the weed infestations and species will likely get worse with time.
Herbicide Resistance in Plants
PUBLIC AND POLITICAL PERCEPTIONS
The main problem in agriculture today is not the technology, but pub-
lic perceptions. There is no significant exposure or risk to human
health or the environment from herbicides in food or groundwater; we
are at serious risk of solving the wrong problem. Ignorance, fear and
emotions must be replaced by education, reason and rational thought
and action. There is the option of dropping herbicide use and purchas-
ing only food produced without them, but we will not remain competi-
tive in world agriculture. We will depend more and more on imported
foods, our surpluses will disappear, we will have less control on the
quality of our food, and the greatest agricultural technology in the
world that is responsible for providing by far the highest quality and
variety of food at the lowest prices that this country or any other has
ever known, will be in jeopardy.
With considerable misgivings, I am prompted to say that what we
most likely need in this country and some others in the developed
world is to experience a little famine. It is only because of our surplus
and efficient production without farmers always being the economic
benefactors that we have such vocal opponents to herbicides. With
only two percent of our population on the farm, our graneries and
supermarkets full, and people who do not have an appreciation for
how sensitive the balance is between feast and famine, some difficult
choices lie ahead. We need to learn to live with herbicides and solve the
right problems.
In summary, nothing will come out of biotechnology, biocontrol
organisms, or other presently perceived and much talked about techno-
logy that will substantially replace chemicals for weed control in the
foreseeable future (20 to 40 years). I hasten to add that there will be
very useful tools and technology developed to help us do better in se-
lecting the more acceptable herbicides, using lower rates, reduce the
leaching and environmental impact of those used, getting more of
them to their sites of action, improve the integration of other control
methods for best management practices, use of biologicals for control
of major or nixous weeds which cannot be adequately controlled with
herbicides, and other improvements for the protection of both crops
and the environment. But just do not try to do it without chemical
herbicides or agriculture will fail to be competitive, profitable, sustain-
able, or environmentally sound.
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