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COFRDA REPORT 3305
Physiological
and
Biochemical
Responses of Plants
to Glyphosate:
a Literature Review
Zwiazek and T..I. Blake
Faculty of Forestry
University of Toronto
1990
Canada-Ontario
Foresi Resource Development Agreement
Entente sur la mis, en valour de la ressource forcstifere
"Minister of Supply and Services Canada 1990
Catalogue No, Fo 29-25/3305E
ISBN 0-662-18154-9
ISSN 0847-2866
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'r
5°" °' "1C aUthOTS ;ind *"" l«
Natural Resources
endorsement bv Forestry Canada or the Ontario Minis,,,, of
Zwiazek, J.J. and Blake. TJ. 1990. Physiological and biochemical
responses of plants to glyphosate: a literature review. For. Can., Oni.
Region, Sauli Ste. Marie, Oni. COFRDA Rep. 3305. 13 p.
ABSTRACT
Current literature on the broad-spectrum herbicide glyphosate |N(phosphonomethyl)-glycincl is reviewed.
The focus is on the uptake,
metabolism and physiological effects of glyphosaie. and on environmental
influences on the herbicide's efficacy and mode of action, particularly as
they relate to coniferous tolerance to the herbicide. H was found that
glyphosate tolerance or susceptibility is a function mainly of uptake,
translation and protoplasmic tolerance, but varies widely among
different species.
This variation cannot be attributed to a single
physiological or environmental factor. This points to the need for
research on each species of interest lo determine the factors most
impoilant for the response of that species to glyphosaie.
RESUME
Les auteurs passenl en revue la documentation actuclle sur le glyphosate
IN-(phosphimomethyn-glycinel, un herbicide non seleclif. Us s'attardent
a Tabsorption, au metabolisme et aux effets physiologiques du glyphosate
et aux facteurs environnementaux influencant Tcfficacite el le mode
d'action de cet herbicide, notamment en ce qui concerne la tolerance des
coniferes a cct herbicide. II a etc decouvert quc la tolerance Oil la
sensibilite au glyphosate esl principalement fonction dc ['absorption, de
la translation et dc la tolerance protoplasmique. mais varie enormement
d'une essence a I'autre. Cette variation ne peut eire attribuable a un seul
facteur physiologique ou environnemental. laissant voii la neccssite
d'effectucr d"autres recherches sur chaque essence en cause afin de
determiner les principaux facteurs intervenant dans les reactions de cette
essence au glyphosate.
in
TABLE OF CONTENTS
INTRODUCTION
1
ABSORPTION OF GLYPHOSATE BY PLANTS
1
2
Season of Application
Water Stress
Differences Among Species
TRANSLOCATION OF GLYPHOSATE IN PLANTS
3
METABOLISM OF GLYPHOSATE IN PLANTS
4
BIOCHEMICAL EFFECTS OF GLYPHOSATE
tic
Synthesis of Aromatic
Amino Acids
4
5
PAL Activity
EPSP Synthase Activity
5
Phenolic Acids
Genetic Engineering
and Tolerance to Glyphosate
Plant Growth Regulators
6
6
Photosynthesis
CONCLUSIONS
7
LITERATURE CITED
9
PHYSIOLOGICAL AND BIOCHEMICAL RESPONSES OF PLANTS
TO GLYPHOSATE: A LITERATURE REVIEW
regrowth of shrubs and other perennial plants
and results in their subsequent destruction.
INTRODUCTION
Glyphosate |N-(phosphonomelhyl}-glycine] has
been widely used as a herbicide since 1971, both
in agriculture and in forestry, ii has a relatively
simple structure and easily forms water-soluble
sails and derivatives, including isopropylamine
sail, used in commercial preparations.
This
literature
review
summarizes
establishment and growth of planted conifers.
However, herbicide lolcrancc varies widely
among coniferous species and individual trees of
the same species (King and Radosevich 1985),
and ulyphosate can have negative effects on the
current
knowledge concerning the effects of glyphosate
on plants, based on a compuier search using the
BIOSIS reference source- The computer search
yielded 25 lilies for conifers and 163 lilies for all
plants.
The level of shrub control significantly affects
growth of conifers.
In the present report we
attempt to summarize current knowledge about
(he mechanisms of ihe action of glyphosate on
planls and the ways in which this herbicide can
adversely affect growth of coniferous trees.
Approximately 40 of llic most relevant
papers arc cited in this review.
Older papers
were obiained from reference lists found in
newer research and review articles, for a toial nl
95 papers cited.
ABSORPTION OF GLYPHOSATE
BY PLANTS
Absorplion and translocalion of glyphosate in
planls are the key factors determining the
response of plants lo this herbicide.
The most
economical, and therefore most frequently used,
technique of glyphosate application is foliar
spraying.
The effect of foliar application
depends on many factors, including the rate of
0-{phmphmiomet!iyI}~gly€ineJ
glyphosate application, droplet size (Ambach and
Ashford 1982. Buhlcr and Burnside 1987).
concentration (Boerboorn and Wyse 1988), the
presence of adjuvants (Richard and Slife 1979.
Glyphosate appears to be environmentally safe
Sherrick el al. 1986, Bovey and Meyer 19X7).
soil moisture (Moosavi-Nia and Dorc 1979a),
rainfall (Bryson 1987. 1988). humidity (Wills
because of ils speed and pattern of degradation
(Tale and Alexander 1974, Sprankle et al. 1975a)
1978. McWhorter et al. 1980), light intensity
(Moosavi-Nia and Dore 1979b, Schultz and
as well as ils low loxicily to animals and people
(Atkinson 1985). Glyphosaie is used as a broad-
Bumside 1980), growth stage (Neal el al. 1985),
cuticular permeability (Wyrill and Burnside
spectrum, postcmergence herbicide to conirol
vegeiation before and at the time of planting. Il
et al. !LJ76. Brecke and Duke 1980).
is particularly useful for control of perennial
weeds because it is readily translocated lo the
There
roots, where it accumulates (Sandberg et al.
1980, Schultz and Burnside 1980). This prevents
1976), and plasmalemma permeability (Gottrup
is no agreement about
the effect of
temperature on glyphosate activity in planls.
N'lcWhorter et al. (1980) found thai increased
temperatures resulted in increased absorption of
glyphosate by johnsongrass (Sorghum fialepense)
and decreased absorption by soybean {Glycine
max). On the oilier hand, Devine el al. (1983)
showed that increasing the temperature had no
effect on glyphosale absorption by quackgrass
{Agmpyron repens). Lowering the tempera lure
also produces variable effects,
Exposure of
quackgrass to a temperature of -4"C had no
effect on glyphosate toxicity, but when poiato
{Solanum luhcrostun) plants were exposed to a
low-temperature regime (13/4"C, day/night),
glyphosate phytotoxicity was lower than in plants
grown
at
higher
temperatures
of
application
to
spring
and
summer
treatments.
absorption.
Water Stress
The effects of growth rate and physiological
Season of Application
season
response
Severe injury caused by herbicide always
occurred when photosynthclic rates were high,
xyiem water potentials were low and shoots were
actively growing. The authors explained the
seasonal nature of herbicide activity in conifers
as being the result of differential absorption
through leaves and restricted distribution after
(24/13"C)
(Masiunas and Weller 1988].
["he
These conifers were found to be more loleranl of
herbicide applications after fall dormancy, with
substantial injury and mortality occurring in
slams
affects
the
susceptibility of plants io glyphosate in different"
ways. Glyphosate appears to have the least
effect on conifers when sprayed in the fall
(Ahrcn.s 1974, Bing 1974) and dormant conifers
can tolerate high doses of this herbicide (Lund-
Hoie 1975, Ahrens 19X1). On the other hand,
deciduous trees are more susceptible to
glyphosate applied in the fall than in the spring
(Putnam 1976, Weller and Skroch 1983). Neal
et al. (1985) examined in detail the effects of
growth stage on glyphosate absorption and
transport in ligustrum (Ligustrum japonicum) and
blue Pacific juniper {.lunipents conferta). The
authors showed that differences among species in
overall (olerancc, as well as in seasonal
tolerance, of glyphosate were a result of
differential absorption rather than of transport of
the herbicide into the plant. Juniper plants
absorbed significant amounts of "C-glyphosatc
only when the herbicide was applied at the time
of shoot elongation.
Ligustrum absorbed
relatively more l4C-glyphosate. mostly during
bud-break and shoot termination.
Seasonal variation in glyphosate tolerance of
on
injury
attributable
io
herbicide
application were studied in ponderosa pine and
an
associated shrub, greenleaf manzanita
(Antostaphylos panda),
by
Paley
and
Radosevich (1984). As in previous studies, the
maximum damage to both species occurred after
spring and summer applications of glyphosate.
Damage caused by glyphosate was well
correlated with growth rale and \ylem potential
in ponderosa pine, bui only with xylem potential
in greenleaf manzanita. The authors concluded
that herbicide selectivity is greatesl when pine
has ceased growing, at a lime when xylem water
potential is low in pine and high in manzanita.
The relative tolerance of some waier-stressed
plants to glyphosate can probably be attributed to
reduced uptake as a result of stress-induced
stomatal closure. DeGennaro and Weller (1984)
attempted
to
correlate
the
differential
susceptibility of field bindweed (Convolvulus
arvensis) biotypes to glyphosate wiih leaf-surface
characteristics. The authors found no correlation
between the differential response and the
numbers of slomala and epidermal cells.
However, they did not measure stomatal
openings, and the gas-exchange rates may not
have been the same in the different biotypes.
ponderosa pine {Finns ponderosu). Jeffrey pine
(Punts jeffreyi), sugar pine (Pinus lambertiana),
Douglas-fir (Pxeitdotxit»a menziesii). white fir
(Abies t-oncalor) and red fir {Abies magnified)
was described by Radosevich et al. (1980).
2
Differences Among Species
Differences in the rates of glyphosate absorption
by plants may explain differences in their
tolerance of this herbicide. Monocots are known
to absorb glyphosate rapidly (Spranklc el al
1975b) and they arc generally very susceptible to
glyphosate
treatments.
On the
other hand,
absorption by woody plants, including conifers,
is generally
interesting
absorbed
slow
thai
by
(Lund-lloie
the
amount
woody
plants
1979).
of
It
is
glyphosate
appears
to
be
independent of the thickness of the leaf cuticle
(Lund-Hoie 1976, 1979).
Cuticle thickness and
that influence plant transpiration (Gottrup el al.
1976. Lund-lloie 1983). However, glyphosale in
plants must be transported through the symplast;
if not, it cannot be exported from leaves.
Rapid
translocalion of glyphosate to roots indicates that
it is transported through the phloem.
glyphosate
was
found
to follow
Indeed,
closely the
"source to sink" pattern, but some glyphosale
was also found to move from the phloem to the
xylem
and
into the apoplast
along
with the
composition are known to be the major factors
transpiration stream (Dewey and Appleby 1983,
controlling
Jachctta el al. 1986).
the
absorption
of
other
polar
herbicides (Kirkwood 1978). Lund-Hoie (1980)
explained high glyphosate tolerance of conifers
The
"source
to
sink"
pattern
of
glyphosate
as resulting exclusively from restricted needle
iranslocation indicates that the
penetration, and many studies appear to support
growing parts of plants should accumulate most
this hypothesis.
Restricted needle penetration
can explain why actively growing shoots of
conifers are susceptible lo glyphosaie and why
those
factors
that
promote
stomatal
closure
reduce the toxic effects of giyphosate.
hypothesis,
however,
does
not
this
explain
the
most actively
of the herbicide and be the first to sustain injury.
A direct relationship between sink activity and
l4C-glyphosate translocation was documented by
Lolas and Coble (1980). Prasad (1983) showed
that most of the '^C-glyphosate applied to
speckled alder (Alnus nigosa) and white birch
different pattern of absorption exhibited by other
(Hcuria papyri/era) was concentrated in growing
woody plants, as illustrated by the ligustrum
example in the study by Neal et al. (1985).
Clearly, more studies are required lo explain the
and Crabtree (1986) showed that roots, immature
roots, active buds, and young foliage.
rhizomes,
and
tubers
of
yellow
Pereira
nutsedge
varying susceptibility of different types of woody
(Cyperus esculentus) accumulated two to three
plants to glyphosate.
limes more glyphosate than comparable mature
tissues. Keeley et al. (1985), also working with
yellow iiulsedge. found that glyphosate was more
readily transported to young, 2-week-old lubers
TRANSLOCATION OF
GLYPHOSATE IN PLANTS
than to those 4 and 6 weeks old.
Glyphosate uptake by plants appears to be by
older
passive
diffusion
and
is
concentration {Gougler and
Translocation
of l4C-glyphosate was also found to be less in
dependent
on
Geiiier 1981).
(15
lo
20
cm
tall)
barnyard
grass
(Echinochloa cruss-gaHi) than in younger (5 to
10
cm
tall)
plants
(Ahmadi
et
al.
1980).
Uptake can be influenced by the chelating effects
DeGennaro and Weller (1984) reported similar
of certain mineral ions (Sandberg et al. 1980).
findings for field bindweed.
but
Burton
and
Balke
(1988)
found
that
glyphosate uptake by suspension-cultured potato
Water stress can
cells was either unaffected or was induced by the
glyphosate in plants, thereby alleviating its toxic
presence of CaSO4, MgSO,. MnSO4. ZnSO. and
effects.
CaCI,
The
also
affect
Iranslocation
oi"
Ahmadi ct al. (1980) investigated the
effects of water stress on the absorption and
translocation of glyphosate in barnyard grass and
binding
of
glyphosate
lo
cellular
found that both processes were affected by low
components, including the plasmalemma and cell
soil-moisture levels.
walls, is very weak (Richard and Slife 1979).
did not measure actual levels of water stress in
and
contributes
to
apoplastic
movement
of
glyphosate. Hence, the distribution of glyphosate
in plants is partly determined by those factors
the plants.
Unfortunately, the authors
Other factors that
influence
the
transport of assimilates in plants are also likely
to
influence
the
phytoloxicity of glyphosate.
3
However, when Masiunas and Weller (1988)
investigated the effects of low temperature and
light on glyphosate absorption and translocation
in potato, they found that low temperature affects
absorption rather than transloeation and thai light
has no effect on the toxicily of glyphosale.
In
woody
plants,
considerable
amounts
of
glyphosate arc transported in the transpiration
stream to the places of most rapid transpiration,
and from there glyphosate is rclranslocaicd lo :he
meristems oi' the youngest shoots (Lund-Hole
I'JK5). As a consequence of this distribution
pattern, the first symptoms of injury caused by
glyphosate in conifers appear in the top shoots
and in those shoots that are actively growing.
The author explained the seasonal activity in
conifers as resulting from the differentia!
absorption of glyphosate through leaves and
restricted redistribution after absorption.
IN PLANTS
Few studies have been undertaken to investigate
glyphosate metabolism in plants, although the
has
been
Coupland (1985).
thoroughly
process in higher plants.
found
Some authors have
aminomethylphosplionie
acid
in
glyphosate-treated plants (Lund-Hoie 1976.
Putnam 1976. Sprankle el al. 1978. Sandberg el
al. 1980), whereas others could find no evidence
of glyphosate degradation (Coupland and Caseley
1979, Marquis et al. 1979, Devine and Bandeen
1983). It is possible that not all higher plants
are
capable
alternatively,
of
degrading
the
presence
glyphosate;
of
amino
methylphosphonic acid in some plants could be
explained by root exudation of glyphosate. its
degradation by soil microorganisms to aminomethylphosphonic
acid
and
subsequent
absorption of aminomethylphosphonic acid by
the roots.
Woody species appear to have a more complex
glyphosate metabolism than the one described
METABOLISM OF GLYPHOSATE
subjeci
microorganisms (Rueppel el al. 1977). but there
is some controversy aboul the importance of this
reviewed
by
Glypiiosate is metabolized
above. Lund-Hoie f 1976. 1979) detected seven
metabolites in Norway spruce (Picea abies}, ash
{Fraxinns
excelsior)
and
birch
{Betulu
verrucosa).
The author suggested
that
glypluisale is conjugated with natural plant
products and transported in this form, with the
metabolite slowly degraded back to glyphosate.
very slowly in higher plants and forms various
metabolites or degradation products.
BIOCHEMICAL EFFECTS OF
Rueppel et al. (1975a,b) showed that the main
metabolic
breakdown
reaction
in
corn
(Zea
mays), soybean and wheat (Ttiticiim aestivitm)
plants is the splitting of the carbon bonds
through hydrolysis and decarboxylalion.
The
authors
proposed
metabolic
pathways
of
glyphosate in plains in which glyphosate is
metabolized to glyoxylate and aminomethyl-
phosphonic acid. Glyoxylate is further degraded
in the glyoxylic and cilric-acid cycles ami is
metabolized into natural plant products, whereas
aminomethylphosphonic
acid
formylphosphonic
which,
acid
is
degraded
Lo
in
is
turn,
converted to formaldehyde, the substrate for a
number of natural plant products.
The degradation of glyphosate to aininomelhylphosphonic acid is well established for soil
GLYPHOSATE
Synthesis of Aromatic Amino Acids
Studies on the mode of glyphosate action in
plants were pioneered by Jaworski (1972]. The
author treated duckweed {Lemna gibba) plants
with glyphosate and various amino acids and
noticed that growth inhibition caused by the
herbicide can be alleviated by the addition of Lphenylalanine
to
the
nutrient
medium.
Treatments with other amino acids did not
produce
significant
reversals
of
growth
inhibition. Glyphosate treatment also resulted in
a reduction in the endogenous phenylalanine
levels in the free amino aeid pool in Lemna and
in the increase in total free amino acids. On the
basis of these findings, the author suggested that
glyphosate
promotes protein breakdown
and
inhibits the biosynthesis of aromatic amino acids
by repressing the activity of chorisrnate muiase
phenytalanine ammonia lyase (PAL) activity by
and/or prephenate dehydratase.
treatments
glyphosate.
resulted
Although
Jaworski's
(1972)
findings
were
supported by the results of many later studies,
They
of
in
an
exlraclable
observed
dark-grown
increase
PAL
24
to
that
glyphosate
maize
in
48
reduction in growth occurred.
the
seedlings
activity
hours
before
of
a
Similar increases
for
in the in vivo PAL activity were observed in
glyphosale action, have not been widely accepted
cuhured I'erilia cells (Ishikura and Takeshima
and the enzymes proposed by the author have
1984) and
proven 10 be insensitive lo glyphosale (Roisch
1980, Hoagland el al. 1979]. but the induction
and
could
his
conclusions,
Lingens
as
well
1974).
as
the
model
The glyphosaie-induced
reduction in free-pool sizes of aromatic acids has
been observed
including
in a variety of plant species,
soybean
(Hoagland
et
al.
1979),
not
in soybean seedlings
be achieved
(Duke ei al.
in the in
vitro tests.
However, Hollander and Amrhein (1980) found
that glyphosate had no effect on the activity of
PAL extracted from buckwheat.
Studies using
buckwheat (Fagopyrum esculennim) (Hollander
PAL inhibitors lo reverse the loxic effects of
and Amrhein 1980). bean (Phaseolas vuigan's)
glyphosate have not been very successful.
(Shaner and Lyon
el al. (1980) found only marginal reversal of
1980). wheat (Triticum sp.)
Duke
of
glyphosate-induced growth inhibition in soybean
Cryptomeria and Perilla (Ishikura el al. 1986).
when plants were treated with a PAL inhibitor,
Haderlic el al. (1977) found thai glyphosale had
amonoxy-d-phenylproprionic acid, and Cole et al.
no effect on the aromatic-acid content ol cultured
(1980) found that PAL inhibitors had no effect
carrol (Damns sp.) cells, bill this may be a result
on the loxieily of glyphosate.
of differences in the growing conditions of cells
appears that glyphosale indirectly interferes with
(Nilsson
1977).
and
cultured
culls
Therefore, it
PAL and that the induction of PAL activity is
in suspension culture.
not a major cause of the toxicity of glyphosale.
The
reduction
in
free
aromatic
amino
acids
appears to be a major result of glyphosate action
and
numerous
studies
have
confirmed
that
EPSP Synthase Activity
supplementary feeding of aromatic amino acids
io plants alleviates the deleterious effects of
Steinruckcn anil Amrhein (1980) observed that
g]yphosate (Shaner and Lyon 1980. Ishikura el
glyphosale
al. 1986. Creswell et al.
However, in
phosphate synthase (EPSF synthase). and they
other studies, the addition of aromatic amino
hypothesized that this inhibition is responsible
acids
failed
symptoms
levels
of
Hoagland
Evidently,
to
19881.
alleviate
despite
a
aromatic
decrease in endogenous
amino
1978. Cole et al.
either
glyphoxate-induced
the
acids
responses
vary
are
caused
by
the
for many of the observed metabolic changes in
plants.
The target enzyme of glyphosale. EPSP
and
synthase. is a critical enzyme in the biosynthesis
of aromatic amino acids, since il catalyv.es the
among
plants or else not all the effects produced by
glyphosate
5-enolpyruvylshikimate-3-
1980).
(Duke
1980. Lee
inhibits
depletion
of
addition
of
the
enolpyruvyl
moiety
of
phosphoenolpyruvale to shikimate-3-phosphate.
Inhibition
of
EPSP
synthase
activity
would
therefore prevent the synthesis of chorismale-
aromatic amino acids.
derived
aromatic
amino
acids
and secondary
metabolites.
PAL Activity
An
alternative
phyiotoxieity
theory
llial
of glyphosate
may
was
explain
the
Phenolic Acids
proposed by
authors
In addition lo lowering the levels of aromatic
suggested that lower levels of aromatic amino
amino acids, the inhibition ol' EPSP synthase
acids
activity rcsuils in elevated levels of shikimic acid
Duke
and
are
Hoagland
a
result
(197X).
of
the
The
induction
of
(Amrhein el al. 1980, Berlin and Wiite 1981}.
The levels of shikimic acids are often higher
than iniglii be expected because lowering the
levels of products of the shikimic acid pathway
results in a deregulation of carbon flow into the
shikimic acid pathway (Jensen 1985).
Levels of other phenolic acids were also found to
increase
Ishikura
shikimic
cultured
result of
(1988)
in glyphosatc-trented plant cells.
et al. (1986) found that, in addition to
acid, quinic acid accumulated in
cells of Cryptomeria and Perilla as a
glypliosate treatment. Lydon and Duke
reported
increases
in
shikimic,
proiocatechoic.
gallic
and
4-hydroxy-benzoic
acid levels in plants of several species treated
with glypho.sate. whereas ievcls of vanillic and
syringic acids remained unchanged. Canal et al.
(1987a) observed an increase in benzoic acids
(gentisic. hydroxybenzoic, salicylic and vanillic)
and a decrease
in cinnamic acids in yellow
nutsedge.
The aulhors also measured PAL
activity in plants irealed with 0.1. 0.01 and
0.0001 M glyphosate and observed a decrease in
activity only after the 0.01-M treatment. This
indicated only a marginal involvement of PAL in
the action of glyphosate.
Glypliosate can also inhibit the synthesis of other
phenolic compounds. Ishikura et al. (1983) and
Teramoto and Ishikura (1985) found that
glyphosate treatments u( Cryptomeria and PcriUa
cell cultures resulted in a marked suppression in
the formation of flavans and caffeic acid, even at
glyphosate levels that were only slightly
inhibitory to cell growth.
Levels of soluble
proteins in Cryptomeria were not affected by a
shorl-term 2-mM glyphosate treatment.
substantial
enhancement
of
EPSP
synthase
activity as a result of overproduction of the
enzyme.
Klee
et
al.
(1987)
cloned
an
Arabidopsis thaliana gene that encodes EPSP
synthase to obtain glyphosate-tolerant plants.
The Arabidopsis gene is highly homologous to
the petunia gene within the mature enzyme and
contains seven introns that are a: exactly (he
same positions as those in petunia, hut which arc
smaller, so that the size of the gene is reduced.
The authors fused the gene to the CaMv 35-S
prometer. reproduced the chimeric gene into
Arabidopsis and obtained overproduction
of
EPSP synthase. which led to glyphosate
tolerance in transformed callus and plants.
Tissue-culture techniques have also been used to
select for glyphosate-toleram lines. Nafziger et
al. (1984), Steinrucken et al. (1986) and Creswell
et al. (1988) selected glyphosate-toleranl cells
grown
in
suspension
culture
and
correlated
glyphosate tolerance with the oveqiroduction of
EPSP synthase.
However, more studies are
needed to confirm the pattern of inheritance and
the stability of these genetic changes in
regenerated plants.
More recently, glyphosate has been shown to be
involved with yet another shikimic acid-pathway
enzyme. Pinto e: al. (1988) studied the effects
of four glyphosate concentrations (0.5. 1.0, 1.5
and 2.0 mM) on the activity of 3-deoxy-</arabino-hcptulosonate-7-phosphaie
synthase
(DAMP synihasc)
solution
culture,
in
and
potato cells grown
showed
thai
all
in
four
concentrations markedly increased the in vivo
activity of the enzyme by increasing the amount
of the enzyme.
The authors used the same
glyphosaie concentrations to study the in vitro
Genetic Engineering and Tolerance to
Glyphosate
Genetic manipulations that have produced
glyphosate-tolerant plants provide more evidence
that the inhibition of EPSP synthase may explain
glyphosate toxicity. Shah et al. (1986) cloned a
gene for petunia (Petunia sp.) EPSP synthase
and used it to engineer glyphosate tolerance by
fusing a cDNA clone lo the cauliflower mosaic
virus (CaMv) 35-S promeler: this resulted in
effects on DAMP synthase and did not observe
any change in the enzyme's activity. Therefore,
the induction of DAI IP synthase activity in
response
to
the
herbicide
probably
occurred
indirectly, by the induction of de nova protein
synthesis.
Plant Growth Regulators
The two major metabolic changes induced by
glyphosaie arc disruption of protein synthesis and
formation of secondary compounds.
However,
marked
inhibition
(at
low
glyphosate
glyphdsate has many oilier effects of potential
concentrations)
importance to plants.
concentrations) of CO, uptake by detached flax
One of them is the effect
on indoleacetic acid (IAA) content.
Lee (1982)
and
induction
(Linum ttsitatissimum) cotyledons.
(at
high
Ireland el al.
and Lee et al. (1983) found that IAA levels in
(1986) studied the effect of glyphosate on the
tobacco callus culture decreased in response to
kinetics of induction of photosynthesis in wheat
glyphosate treatments.
leaves and determined that neither the rate of
The authors concluded
that this decrease was the result of accelerated
carbon
oxidative degradation of IAA and the formation
emission was directly affected by glyphosate
of conjugates.
treatment.
In other studies it was found that
IAA levels increased in glyphosale-trcaicd planis
(Canal cl al.
Canai et al.
1987b. Rajesekaran et al.
1987}.
(1987b) quantified IAA in yellow
nulsedge leaves and attempted lo correlate an
increase in IAA with a rise in gentisic acid
levels.
The authors hypothesized thai elevated
levels of phenolic compounds
in glyphosatc-
ireated planis help to protect IAA from oxidation
by inhibiting IAA oxidase activity. Although the
authors were not able lo measure IAA oxidase
activity
in extracts from control
and
treated
planis, they found elevated IAA and gentisic acid
levels and demonstrated in vitro that genlisic
acid inhibits IAA oxidase isolated from nutsedge
leaves.
However, changes in IAA content can
also be caused by a direct inhibition of IAA
transport by glyphosate (Baur
interference
of
accumulation
1979) or by the
glyphosaie-induced
(Cole
et
al,
1983)
fixation nor the
The
glyphosate
level
authors
affects
of chlorophyll
concluded
photosynthetic
that
induction
kinetics by an indirect modification of carbon
metabolism.
A marked inhibition of net carbon exchange has
been reported for sugar beet (Beta vulgaris) by
Geiger el al. (1986, 1987). Gciger et al. (1987)
showed that photosynthetic inhibition in sugar
beet was
not caused
by changes
in stomaial
conductance because internal CCK levels were
not affected by a glyphosate-induced reduction in
slomatal conductance. The authors constructed
two
hypotheses:
that
glyphosale
may
inhibit
regeneration of biphosphale carhoxylase or that
glyphosate limits ATP or NADPH production.
Unfortunately, they presented no evidence in
favor of either mechanism.
ethylene
with
IAA
transport.
CONCLUSIONS
Glyphosate is a potent herbicide that probably
lias more than one site of action in plants.
Photosynthesis
tolerance of some plants to glyphosate may be
Glyphosate is considered to be a non-photosyn-
theiic herbicide.
Sprankle et al. (I975b> found
no initial effect of glyphosate on photosynthetic
rates in Agropyron repens until 72 hours after
exposure.
The
The assimilation rate of soybean leaf
explained
translocalion
by
(i)
or
(ii)
restricted
uptake
protoplasmic
and
tolerance.
Bvidence for the latter mechanism was found in
those cells that overproduce EPSP synthase. The
response of plants to glyphosate appears lo be
controlled by many factors and varies among
cells was also found to be relatively unaffected
plant species. Therefore, the conclusions reached
by
in studies conducted with one species may not be
glyphosate
(Tymonko
and
Foy
1978).
Podesta et al. (1987) also failed to show changes
valid for other planis.
in phosphocnolpyruvate carhoxylase activity in
conducted on conifers; hence, little is known
glyphosaic-trcated maize (Zca mays) leaves. On
about how glyphosate interferes with metabolism
the other hand.
in coniferous trees.
Cole cl
al-(1983)
showed a
Few studies have been
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