Download plants - Natuurtijdschriften

Acta
Bot. Neerl. 41(3), September 1992,
p.
229-248
Review
Metal tolerance in
plants
W.H.O.
Verkleij and
J.A.C.
Ernst
H.
Schat
Department of Ecology and Ecotoxicology, Faculty of Biology, Vrije Universiteit,
De
Boelelaan
1087,1081 HV Amsterdam, The Netherlands
CONTENTS
Introduction
229
Measurement of metal tolerance
230
Comparative plasmology
231
Rooting technique
231
Whole
232
plant testing
Compartmentation
and tolerance
at
the cellular level
232
The cell wall
232
The plasma
234
membrane
Membrane structure
The
234
kinetics
Uptake
235
cytosol
236
Enzymes
236
236
Metallopeptides (phytochelatins)
Organic
Vacuoles
acids
as
238
238
storage compartments
the whole plant level
240
Allocation pattern of metals and leafage
240
Reproductive
240
Compartmentation
The
costs
at
organs
of metal tolerance
241
References
242
INTRODUCTION
Nearly
when
60 years ago, Prat
he
was
analysing
(Melandrium sylvestre),
able
to
demonstrate
non-mine
Nearly
20
ecological
a
population,
years
and
(1934) initiated
the
laris in the
later Bradshaw
synonymous
Smith, Thlaspi
a
explained
(1952)
species
as
a
caerulescens
Sibth., Silene
J. et C.
from
been
T.
alpestre
Meyer.
229
L.
(1954)
plants
1959; Gregory
vulgaris (Moench.)
Presl. with
populations
a
were
in
plants
of Silene dioica
non-mine soil. He
population,
result of evolution
study
frequently investigatedplant species have
A. tenuis
one
and Baumeister
chosen for
(Jowett
heavy metal resistance
two
resistance in the mine
differentiationbetween
physiological
with
of
copper mine and
copper
which he
Bradshaw group
Note. Some of the
is
from
one
heritable
contaminated habitats. The
the research of
growth performance
by
relative
was
the
to
natural selection.
started further research
from metal-enriched and
on
non-
predominantly Agrostis capil-
1965; McNeilly
taxonomically
Garcke with
1965;
renamed.
Agrostis capillaris L.
S. cucubalus Wibel
and Noccaea coerulescens
Antonovics
(J.
and S.
et C.
inflata
Presl.)
F.K.
230
W.
1966)
and Silene
Riither
1966).
the
O.
in the Baumeister
vulgaris
In
H.
late
1950s
one
and introduced the
In the 1950s, the
plant
techniques
as
phase
separation
i.e.
laboratory-raised plant material,
after
1969). Only
material (Reilly
The
research
atomic
applying
in
the
(Turner
in the vacuole (Reilly
within the
late
&
Ernst
enzymes and
metallo-enzymes
non-resistant
plants
ing
led
(Ernst
distinctly
tolerant
nearly
Ten Bookum
and
on
the
leaves,
on
phytogeographic
&
on
plant
possible.
of metals
(sub)cellular-
(zinc)
the cell
to
and metal accumulation
to
for
1967; Peterson
of
study
either time-
wet-ashed
become
the
by
was
applicable
Gregory
analyses
binding
were
only
translocation from root
1969). Also,
or
analysis
costly
or
characterized
(Zn, Cu)
shoot, allocation
and activities of metal-stimulated
studied. Observed differences between resistant and
of various
development
populations
vegetation
metal concentrations in
spectrophotometry
accumulation in
all of them
in the resistance
possible only
metal
1964),
studies
isogenic
of
study
the
using
physiological
From the
(Ernst 1975; Mathys 1975a).
resistance,
a
metallophytes.
radiolabelling (Turner
was
were
the
to
approaches
1964; Gries 1965;
the
studying
measuring
available for
number of groups became involved in the
of metal
for
Gregory 1967; Peterson 1969)
1967;
1962; Ernst
H. SCHAT
physiological aspects of metal resistance
absorption
1960s
shoot, age-dependent
metal resistances
processes in
techniques
compartmentation patterns, particularly
wall in grasses
the above
did time and cost-effective metal
1967)
C, VERKLEIJ AND
while
(1958),
to
of evolutionary and
The
samples.
such
consuming,
study
speciation
the absence of convenient
hampered by
small
of
study
A.
group (Broker
Duvigneaud
metalliferous soils in Central Africa, added
J.
ERNST,
a
metals
models for
onwards,
and
physiological
rewarding approach
lines of
to one or more
1970s
early
of
specific
increas-
genetical aspects
comparison
a
which differ
single species
& Macnair
(Strange
an
as
far
of
as
1991; Schat &
1992a).
The present review
will
mechanisms of resistance
highlight
to
the
the progress with respect
heavy
metals Cd,
Cu,
the elucidation of the
to
Pb and Zn, and the metalloid As in
angiosperms.
MEASUREMENT
OF
of whether it lives in
Every organism, regardless
a
certain ability
although
there
(Bradshaw
&
to
cope
are
increase in the
limits in the
ability
limited number of
Pb
(Urquhart
1992a),
As
dependent
al.
1971;
occur as
on
to
a
excessively
cope with excessive
to
to
restrict these
or
and
species
Macnair
this
a
lot of
ability
as
terms to cases
metal, usually naturally
or
higher plants
‘tolerance’
of
a
rapidly
as
1976),
within 5
the selection pressure
and
to
Cu
(Macnair
other metals.
10 years (Ernst
prevailing (Dueck
1983;
selected
occur
(Broker
in
1962),
Schat & Ten Bookum
Evolution of tolerant popu-
1976;
etal.
or
heritable
artifically
have been demonstrated for Zn
1991)
not, has
available essential metals
toxic level of metal exposure. Such heritable tolerances
plant
&
or
of metal tolerances in
wish
we
Wu & Antonovics
(Watkins
lations may
occurrence
metal-enrichedenvironment
Several authors have referred
review, however,
under the pressure of
a
with non-essential metals
McNeilly 1991).
‘resistance’. In this
a
METAL TOLERANCE
Wu
1984;
1990),
Dueck
or more
slowly,
1986; Verkleij
et
1989a; Lolkema 1985).
Tolerances
to
metals
metal tolerance is
plant.
It
is
Antonovics
a
can
maintained in
1978; Qureshi
tissues, organs,
or
be demonstrated at different levels of
constitutive property, present in
every
cell
et
the whole
al.
tissue
cultures
prepared
1981). Therefore,
plant, although
it
from
tolerance
cannot
cell,
can
integration. Basically,
tissue and
organ of the
tolerant
plants
be tested
using
(Wu
&
different
be excluded that processes
taking
METAL
place
TOLERANCE
at integration
of the whole
IN PLANTS
levels
231
than the cell
higher
may
contribute to the tolerance
substantially
plant (see below).
Comparative plasmology
elaborated
Repp (1963)
a
metals. Sections of leaf or
for
test
membrane
plasma
tissue,
stem
layers thick,
series of metal concentrations, either without nutrient addition
in
nutrient solution
a
48 h for all other
1
using
(Riither
glucose. The advantage of
m
in
with
agreement
Ernst
this
those
to
without
laboratory
with
the
rooting
of
case
testing
a
or
or
copper,
is tested
deplasmolyse
is that it allows
technique
obtained
and
plasmolyse
heavy
to
incubated in
are
(Repp 1963; Gries 1966)
After 24 h in the
1972a).
ability
in the field and in the
dicotyledonous plants
are
1967;
the cells’
heavy metals,
after exposure
integrity
between 2 and 4 cell
of established
them. The results
cloning
described
technique
below
(Ernst 1982).
Rooting technique
Roots
are
case
responds
more
that
growth
root
used
measure
confronted with
directly
more
except in the
of aerial metal
rapidly
is the
to
of tolerance is the tolerance index TI
of TI
of this
testing,
allows
certainly
as
well
as
the
at
single
such
use
a
of
a
depends
& Ten Bookum
presumed
ation in tolerance, it
Mimulus guttatus
clear-cut
EC,
00
as
a
homozygote (his
measure.
The
this
a
is
completely
quantitative
measures
fully applied
Bookum
a
review).
in
test
detailed
growth
multiple
The
the
genetics
effectively
yielded
never
identifies the
to
the lowest
[EC I00]).
Schat &
which also used the lowest
exposing
a
presumed
of copper tolerance in
approximately equal
concentration test,
chosen
quantitative vari-
in non-tolerant plants stop
advantage of this
alterna-
an
root, whereas
studies has
more
each individual to
stepwise
test over
variation in tolerance among tolerant
analyse
developed
not measure
test
The latter is established by
arrested.
to
genetical
for
be tested
to
discussion). Moreover,
genetical analysis
Macnair’s
plants
in tolerant plants, which
(1983)
failed
does
concentration was
root
a
a
test
and
The resolution
manner
Macnair’s
plants.
of copper tolerance in Silene
a test
until
test
root
is that
It has been
it
success-
vulgaris (Schat
& Ten
1992a). Compared with conventional multiple concentration tests, it has the
advantage
need for
to
1958):
fixed metal concentration,
to a
of TI in
use
Apparently,
(1992a) developed
tolerance
reason
metal concentration chosen
solution in which the metal concentrationis raised in time in
growth
for
growth, especially
exposed cuttings
1983).
results.
effect concentration (EC) where
Ten Bookum
the
non-tolerants consistently
successfully applied
was
interpretable
non-tolerant
on
1983,
1992a, for
root
rooting. Although
(Macnair
the
commonly
patterns of interspecific
coarse
(Woolhouse
metal-free control solution. Macnair
tolerants showed normal
A
Jowett
(Wilkins 1957, 1978;
of the
perception
is limited and
concentration test. He
level that
a
tests.
in control solution
growth
low metal concentrations may stimulate
questions
probably
the range of variation in tolerance present among the
(Macnair 1981, 1983; Schat
tive
This is
shoots,
growth usually
in metal solution
growth
variation in metal tolerance
index, however,
growth.
root
=
root
use
1980). Therefore,
used parameter in metal tolerance
widely
root
intraspecific
metals in the environment than
metal exposure than shoot
most
TI
The
heavy
deposition (Ernst
that it allows
cloning
to
them. A
estimate the tolerance level of individual
general advantage
of
multiple
plants
concentration
without the
tests over
single
232
W.
concentration tests is
metal tolerance
higher
a
only
are
Nicholls & McNeilly
H, O.
resolution.
tolerance
to
(Macnair
used, but probably
measures
lowest EC
for
100
Schat & Ten Bookum
1992a)
as
the
This
to
a
applies
growth
used,
was
be
may
unrelated to tolerance
genetic
low
1977;
for
testing
growth
root
the
tolerance
use
of the
(Macnair 1983;
to root
in
genetic studies,
factors
growth
root
component parts of TI (Macnair
two
of
sensitivity
in former
explained by disproportional effects of
the
on
all
to
studies
comparatively
factors other than tolerance genes. The lack of success
which TI
1973; Craig
major problem
The apparent success of the
in
SCHAT
concentration tests for
Snaydon
A
AND H.
innate variation in
to
measure
be due
seems to
&
restriction
same extent.
tolerance
a
C. VERKLEU
1992a,b).
sensitive
are
1981).
not to
growth
root
Davies
(e.g.
& Ten Bookum
metal tolerance is that tolerance measures
unrelated
J. A.
Unfortunately, multiple
scarcely applied
1979; Schat
ERNST,
&
1981; Humphreys
Nicholls 1984).
The usefulness of
relies
root
the fact that
on
growth
metal on the
root
itself,
lished
and
experiments
data)
elongation
than
more
are
as an
metal-imposed
such
affected. In
with
Zinc also
protein
Davies
el
Several authors have used the relative
growth
rate
Whole plant
et
tests
(e.g. Verkleij
tolerant plants may differ in the
to store
of shoot
exposed
yield
at
root
rate
whole
phase
division and
3 pM Zn
to
less
cell
results in
a
than 20% in
a
to
appears
be sensitive.
in
non-tolerant and
metal-tolerant
1991a,b).
of the whole plants
1989).
levels of
root
to
the
degree of
so,
growth inhibition,
then whole
a
plant growth
with the
same
test.
clone
produce large
line have
isogenic
COMPARTMENTATION
AND
not
effect
parameter
to
plant testing
test.
For
may be
due to
differences between
published,
TOLERANCE
if
AT
degree
they
a
a
are
to
far
as
THE
rapid
1984).
rooting
tests
stronger
a more
al.
et
plant
as
non-
in the
expected
exhibit
vulgaris
between whole
or
example, compared
plants (Lolkema
been
shoot
also differ in the
vulgaris (Fig, 1), possibly
Systematic comparison
or
an
growth inhibition,
rooting
shoot translocation of copper in the tolerant
not
they might
root
Cu-tolerant Silene
reduction than non-tolerant S.
that this does
as
In view of the fact that tolerantand
of translocation of metals from root
toxic metal concentration. If
growth
to
to
of the meristem and the proximity
metals in the root, it is conceivable that
obvious, however,
tests
& Prast
growth inhibition, relative
to a
equal
Both cell
exposure
the G1
tip
results which differ from those obtained with
shoot
probably
experiments (H. Schat, unpub-
cycle, compared
al.
tests
direct effect of the
a
testing.
in metal tolerance
capacity
rubra,
content
root
I986a,b,c;
populations (Powell
al.
the
to
root
segments.
plants especially,
elements
xylem
split
root
of the cell
length
the
differentially affects
and
isolated
non-tolerant Festuca
100% increase in the
hairs
root
reduction is due to
growth
demonstrated by
as
zinc-tolerant one. In non-tolerant
of
effect parameter in metal tolerance
root
test
and
we
It is
and
a
rooting
know.
CELLULAR
LEVEL
The cell wall
The
walls
of
the
root
cells
are
directly
exposed
to
the
metals
in
the
Association of metals with the cell
wall has been frequently established,
cation
1969, 1972a; Peterson
exchange
Turner
techniques (Ernst
1970; Farago &
Pitt
1977),
or
by
electron
1969; Pickering
polygalacturonic
acids,
to
which
the
affinity
of metal ions
heavy
solution.
& Puia
microscopical techniques
Weinert 1972; Muffineta/. 1985). Most of the cell wall-associated
to
soil
either through
metals
decreases
in
1969;
(Ernst &
are
bound
the
order
METAL TOLERANCE
Fig.
of
fractions
1. Root
IN
PLANTS
(percentage
of total
233
lished).
non-Cu-tolerant
■
of Cu-tolerant and non-tolerant Silene
dry mass)
growth in copper-toxic solution, compared
(Amsterdam),
equal
at
□
levels of root
moderately
elongation
Cu-tolerant
vulgaris
inhibition
(Marsberg),
O
after 7
days
(H. Schat, unpubhighly
Cu-tolerant
(Imsbach).
Pb
>
Cr
>
Cu
cell walls in
The
Zn
(Ernst 1972a,b;
(1969),
observed
capacity
in
a
lead
studies
uptake
of
suggestion
Peterson
1972)
> Ca >
1977). Therefore,
& Pitt
an
from
who
areas
The
amount
The
in
an
disputed (Turner
Jones
et
al.
(1971).
Zn
of the cell wall. This could
not
They
zinc
suggested
of the Australian
concentration. In
of metals bound
(Ernst
& Weinert
metallophytes (Ernst
idea of
such
Cu and Zn from
as
1991).
Turner & Marshall
be confirmed
plant species
general,
to
1972),
the cell wall,
is
usually
even
& Pitt
Polycarpea glabra
a
tolerance-
of cell wall material
when
crystal-like
metal
less than 10% of the total cellular
1969, 1972a,b, 1974).
involvement of the
cell wall in
metal tolerance has been
& Marshall 1971; Ernst 1976; Thurman& Collins 1983;
1990). The main problem is
altered
an
by Farago
there is also
capacity
by
(1971,
Zn-binding
involves
tolerance
variation in the cation exchange
amount
bodies are present in it
De Vos
metals,
that
low
unrelated interpopulation
(Ernst 1972b).
1979;
1972; Muzzarelli 1973; Farago
Sangal
desorb other
correlationbetween Zn tolerance and the cell wall’s
investigated populations
and
al.
et
(1970) and Wyn
positive
high
to
involvement of the cell wall in zinc tolerance has been made
Turner
Agrostis capillaris.
of
Jellinek &
be used
(Harrison
carbohydrate composition
(1977)
can
that it
is
not
easy
to
imagine how
an
frequently
Verkleij
&Schat
increase in binding
W. H.
234
Fig.
2. Model
capacity
the soil
of the
of the cell wall
can
reduce the free-metal
tolerance
suggested
to
cell-wall-bound
such
enzymes
from mine
Poulter
el
al.
waste
as
the acid
the
does
but
mechanism,
A
1983).
the
plasmalemma surface,
are
this
at
& Woolhouse
play
a
a
than
their
equally
tolerant
to
Cu and
cell wall in Pb tolerance. These
to
prevent
a
role in
(Urquhart 1971;
ml of incubation
an
clones may
strongly
Lane
The
et
plasma
Membrane
causes
seems
artefact.
the
by
to
make the
that the apparent
Differences
between
precautions
upon
addition
of cells added per
higher
tolerance of cells
Pb-tolerant and
non-tolerant
elongation,
activity (Mukherji
lAA-oxidase
and cells
role of the
specific
necessary
1976).
amount
acetic acid-induced cell
indole-3yl
by lead, stimulating
structure.
of
cells of
Exposure
potassium
of
plants
higher
1983),
1991).
from the cells,
(Wainwright
plants,
Silene
i.e.
&
which
Maitra
increased concentrations of Cu
originally
as
Agrostis capillaris
vulgaris (De
Vos
In Cu-tolerant ecotypes
leakage (Fig. 2)
are
et
or
much
al.
is
1977;
clones,
between the
highest
leakage,
et
al.
2+
and
Hg
2+
shown for Chlorella (McBrien &
loss has also been observed in
(Wainwright
1989),
higher
& Woolhouse 1977; De Vos
view of the instantaneous occurrence of
similarity
to
Filippis 1979). Copper-induced potassium
induce membrane
able
not
a
in
from Pb-
protoplasts
evidence for
the cell wall. In view of the
possible
occurs
Wu & Antonovics
protoplasts prepared
as
from
membrane
Woolhouse
ones
did
1978).
form
1978).
leakage
& Macnair
taken
authors, however,
of Pb
it
medium,
be caused
Hassall 1965; De
root
binding
experimental
affected
al.
was
metal
It has been
lead tolerance, which
loss of Pb tolerance in
Zn, which
metal-
in
indications that
in the free-lead concentration in the incubation medium
drop
of the cells due to the
represents
to
explain
counterparts
Cox & Thurman
1975;
significant
some
if
Co-ion
of metal tolerant populations
metals
habitat-specific
equilibrium.
cannot
tolerant cell cultures of Anthoxantum orodatum. On the other hand,
were
SCHAT
H.
role of the cell wall
specific
phosphatase
and from roadside soils
observed
(1985)
possible
a
Collins
(Wainwright
claimed that the cell wall
plants
near
processes within the cell wall. There are
with
complexes
uncontaminated soil
as
&
(Thurman
tolerance may be related
stable
activity
the cell wall solution and the cell wall matrix
exclusion has been
less
C. VERKLEIJ AND
tolerance mechanism.
copper
solution,
specific
J. A.
ERNST,
O.
&
Woolhouse
and Mimulus guttatus
the Cu concentrations
than in Zn-tolerant
or
1977;
(Strange
required
to
non-tolerant
1991; Strange & Macnair 1991). In
i.e. within a few minutes, and the remark-
no-effect-concentration
(NEC)
for
K-leakage (Fig. 2)
METAL
and for
TOLERANCE
toxic
Cu
it has been
1991),
Vos
(De
membrane
al.
et
structures
with
Experiments
radical-producing
tolerant
for
plants
the
sulphhydryl
tolerant
are
able
same
channels
general
patch-clamp
to
methods
& O’Dell
1981;
Cakmak &
Horst
of membranes in non-tolerant plants.
It has often been
Uptake kinetics.
of the metal in
observation that
shoots,
metal
although
Lolkema
et
suggested
question,
at
al.
Schat & Kalff
this is
certainly
1984; Verkleij
1992).
not a
rule
contents
tolerant
tissue
plants,
contents
uptake
at
does
performed
but
to
not or
a
in
at
growth
levels have
exposure
exposure levels that
the kinetics of
Comparative
hardly
uptake
copper
in
been
root
higher
a
Cu
uptake
in non-tolerant roots, due
represent passive diffusion
tested
such
by
as
1979)
these
as
a
observed in leaves and
and
result of
authors, however,
roots
do
roots
to a
studies
roots
metal
Further
are not
segments
copper-imposed
not
comparative
transport
in
to
account
for
(Veltrup
a
of
very
to
the
of
non-
differential
a cause,
the kinetics of metal
&
Strange
Macnair
copper-tolerant
similar K
was
and
and V
m
that
term
max
,
considered to
membrane damage. The models
biphasic
1976,
1991;
uptake
Cu
uptake (Nissen
1977),
with
1973),
der Werff& Ernst
a
phase
transition
& Macnair
by Strange
studies of metal-uptake kinetics in tolerant and non-tolerant
date. In
higher plants
metal ions is often assumed
De Vos
toxic
of Elodea nuttallii(Marquenie-van
of Hordeum distichum
available
1989;
conditions,
on
between 6-5 and 7-5 pM, i.e. half the concentration range chosen
(1991).
level of metal
1975; Baker 1978;
are
performed.
linear
the
on
those of the
Moreover, comparisons
rate.
the tolerant ones. Under these
of exposure.
cause
decreased
based
reflect differences in
non-tolerant Mimulus guttatus. Their best-fit model indicated
but
same
al.
et
& Prast
only
not
on a
mem-
not
of differential tolerance, rather than
consequence
a mere
long period
non-toxic
(1991) compared
rarely
or
may
plants.
oxidation
isolated
mainly
the
at
Wu
the
be useful to validate
plants, especially
1972b;
and
in
1991; Slivinskaya
that Zn does
is
soon as
proceed
damage
not
suggestion
1985; Verkleij
however,
have often been
be
may
after
especially
This
(Ernst
& Bast-Cramer
Tissue contents,
Anabaena
As
proteins against
surprising
not
of the tissue of tolerant
contents
may
or
proteins,
K-leakage
that metal tolerances could rely
least in part.
rates, but also differences in translocation
tissue
and
be lower than those of non-tolerant plants grown
may
exposure,
and
1988)
leakage
high
then
De Vos
1991;
Cu
for all Cu-
true
1991).
composition
1991)
of
groups
Vos
free
suggest that Cu-
membrane in Cu-tolerant
lipids
concentration. Therefore, it is
even
uptake
& Prins
membrane
we
the
that
efflux and
bluegreen alga
exceeded,
al.
plasma
reagents
+
of H
hold
seems to
vulgaris (De
are
et
plasma
1987)
sulphhydryl
lipid
Vos
(Maathuis
branes,
at
in
changes
plants (De
zinc protects
copper,
to
Silene
growth
root
and
shown
sulphhydryl
to
from the
rank,
as
have
high sensitivity
This
(Hille 1984).
of structural alterations of the
contrast
with
Strange
effect of
alterations of
(CHP)
& Gonsalves
react
such
al. 1991;
primary
1991).
resistance
In view of the
of their taxonomic
angiosperms,
concomittant
involves
& Macnair
et
is the
jY-ethylmaleimide (NEM)
(Kennedy
in tolerant and non-tolerant
way
(Bettger
to
with
peroxidation
hypothesis
In
1989).
Cu
to
a
Vos
(De
damage
hydroperoxide
to
prevent Cu ions
potassium
1991)
al.
et
tolerance
reagent
due
not
Cu
1989; Strange
no-effect concentrations for
1991). Perhaps
the
to
plants, independent
highest
lipid
is
al.
cumene
polarization
doliolum (Rai et al.
the
et
Vos
(De
that membrane
that
(De
vulgaris
those of
example
and
1989)
Vos
free-radical formation
membrane
235
postulated
compound
tolerance in Silene
plasma
PLANTS
both in tolerant and non-tolerantplants
growth,
root
& Macnair
IN
to
general,
are
be
poorly
the mechanisms of
trans-plasma
understood. Trans-membrane
protein-mediated (Gutknecht
membrane
transport
1983). Specific
of
carrier
236
W. H. O.
for essential
systems
heavy
A clear
metals have
heavy
metals have been
of a reduced
means
& Macnair 1990, 1991a,b; Watkins & Macnair
taken
up
the systems in
by
Agrostis capillaris,
to
Interactions between
is arsenic tolerance (Meharg
uptake
Both
Holcus
of the
and
phosphate
lanatus exhibit
and the
high-
arsenate
are
Arsenate-tolerantplants of
Reay 1979).
and
cespitosa,
decrease in the V
a
SCHAT
1977, 1978, 1979).
1991).
&
angiosperms (Asher
Deschampsia
uptake, due
arsenate
VERKLEIJ AND H.
been found thus far.
not
frequently registered (Veltrup
of tolerance by
example
J. A. C.
ERNST,
reduction in
a
low-affinity uptake
max
and
system
increase in the
an
the reduced
As
high
uptake
concentrations
well-known interaction of
known that
for
except
present
al.
et
pioneer stages
metal ions
are
organic
taken up
(Hall
of
to a
et
toxicity
lesser
et
al.
of
al.
virtually
1992).
absent
On
plants,
al.
1975;
of free
et
al.
1991),
uptake.
containing
prevent the
can
Hassan &
which
species
on
higher
affect the
biocomplexation
be
Coombes et al.
floristic
diversity
metal soils with
heavy
mycorrhizal (YAM) fungi might
possibly through
metals will
1981). Complexed
(Ernst 1968;
the
the
modify
can
heavy
der Werff
explains
Han Hai
ions. It is well
In metal-enriched soils,
1980).
than free-metal ions
Tang
heavy-metal
part of the
development,
1991),
(Dueck
profile
uptake
et
al.
and
1986;
however, vesicular-arbuscular mycorrhizal fungi
copper soils,
(Griffioen
often
metal-binding compounds
Butler
1979;
degree
et
the presence of
of metals in host
letswaart
& Salsac
uptake
variation in metal tolerance of plant
development. Also,
1975; De Koe
complexes (Ernst 1974; Van
1977; Van der Werff 1981; Laurie
greater
consider the
vegetation
metal
phosphate
plants,
with phosphate in glycolysis.
excretion
population-specific
soluble
as
how As-tolerant
uptake (Cathala
1983) usually
for
high-affinity system
explain
& Peterson
(Porter
arsenate
of these metals
availability
are
of the
cannot
studies of metal
Laboratory
1976; Cataldo
and
K
m
However,
very
by
& Ernst
1990),
because of the
fungicidal properties
of this
metal.
The
cytosol
enzymes of tolerant
Cytosolic
Enzymes.
(Woolhouse
& Walker
1981),
are
as
plants (Ernst 1975, 1976;Mathys 1975b; Cox
Therefore, tolerance
metal
in
species
the
must
distribution of essential
&
(Lolkema
Assche &
Vooijs
el
within
heavy
al.
1986)
so
that
Clijsters 1990; Clijsters
et
must
the
At
metal-complexing compounds which
apoplastic
to
ones
those of non-tolerant
activity
the
of potentially harmful
time,
same
guarantee the supply
undesirable metal
al.
as
1976, 1978; Smirnoff& Stewart 1987).
keep
certain limits.
metals
contrast
metal-sensitive
include a mechanism to
cytosol
in
plants, possibly
generally
substitution
the
intracellular
metalloproteins
to
cannot
occur
(Van
1991). This could be affected by the production
may
at
the
same
time promote the transport
to
of
other
cellular compartments.
Two groups of
metal carriers
Rauser & Curvetto
1975a;
Sasse
tolerances
can
most
in
1980) and,
1976).
be
Metallopeptides
present
have been
compounds
during cytosol transport,
In
the
suggested
i.e.
for zinc and nickel,
following
explained by
section
increased
Miranda et al.
as
cytosolic
genes
acids (Ernst
will
discuss
of these
coding
1990; Evans
of the metallothionein-likesubstances
act
organic
we
production
(phytochelatins). Although
higher plants (De
to
metal-binding peptides
(Robinson
et
metal buffers
(Reilly
et
al.
1975,1976; Mathys
whether
metal-specific
compounds.
for metallothioneins (MT)
al.
or
1970;
1990; Tommey
& Jackson
1986),
et
are
al. 1991),
isolated
during
METAL TOLERANCE
the
1980s
early
Lolkema
al.
et
IN
PLANTS
237
& Curvetto
(Rauser
1984; Wagner
Bartolf
1980;
1984;
also
glutamylcysteinyl)glycines (poly(y-EC)„G’s),
phytochelatins
1990)
They
and
et
al.
et
1985a,b)
Rauser
various
by
&
called
1991).
metals and
heavy
cultures
far
so
is based
For free ionic
depends
increases
of
independent
tolerance
EC)
metals the order
more
G’s
n
less
or
(Grill
Rauvolfia
metal-specific
with
proportionally
be
obviously
produced.
Another
of labile
incorporation
a
al.
et
et
al.
factor
into the
sulphur
n,
on
with
al.
et
1981),
(Grill
of metals
to
decreases
in
al.
et
whereas
in
case
the
increase
an
G
metal-(y-EC)
on
in the
conceivable
a
the
(y-EC)„G’s
example,
it
the metal
chain
bearing
order,
medium.
Skoog
of Cu,
it
is largely
concerned,
length
of the
tolerance
on
(y-
order
This
1987).
1989;
induce
of Cd, for
case
al.
et
of metals for
affinity
way. In the
al.
et
(y-EC)„G’s.
1987; Delhaize
1990). Therefore, depending
dependent
1980;
non-metals selenium and
serpentina
be different. The
may
but in
n,
(Matsumoto
n
might
the
the total metal concentration in the Linsmaier and
on
the value of
on
they
by
even
Hg> >Cd,As,Fe>Cu,Ni>Sb,Au>Sn,Se,Bi>Pb,Zn
however,
Jager
probably poly(y-
are
will be named
1991). The tendency
of
&
Weigel
1986)
cadystin (Murasugi
In this review
Goldsbrough
cell-suspension
1980;
metal-binding polypeptides (Jackson
or
plant species investigated
1989; Gupta
in
EC)„G's
al.
peptides (Me-BC;
in all the
arsenate
Salt
(PC;
induced
are
Grill
al.
et
Robinson & Thurman
is
(ythe
complexes (Steffens 1990).
n
There
many indications that
are
tolerant
First,
plants
ones
(Verkleij
case
of exposure
et
tolerant
EC)„G’s
high
to
inhibition
(Schat
should be taken
that
imply
stress
is
&
et
al.
This
1991).
G
(y-EC)
be used
as
a
equal degree
differential
correlated and
any
metal-specific
and
cannot
metal,
of
non-
of
amounts
(y-
growth
root
(y-EC)„G production
biomarker of metal
tolerance-independent
against
a
role for
for
account
in metal
(y-EC)„G’s
metal-specific
n
because it can be induced by
at
of differential tolerance. It would
cause
Another argument
production
produce equal
cause an
that
suggests
a
in the
only
occurs
1992). Moreover, distinctly copper-tolerant
consequence, rather than
can
(y-EC)„G production
lines of the latter
species
1992).
levels
than non-tolerant
1992). Secondly,
both in tolerant and non-tolerant plants
possible,
not even
concentrations which
at
Kalff
a
Verkleij
that
is
involved in metal tolerance.
(y-EC)„G’s
more
al. 1992; Schat & Kalff
et
maximum
levels,
isogenic
grown
&
as
Vos
and
(y-EC)„G
(Ernst
tolerance
growth
vulgaris (De
are
copper
not
are
produce
not
al. 1989a,b, 1990; De Vos
populations
if they
cells often do
or
concentrations where
of Silene
phytochelatins
tolerances,
both in tolerant and non-tolerantplants. Tolerance-
increases in
(y-EC)
G
inducibility
have
never
been found
to
n
date.
as
Thus,
if cadmiumtolerance would rely
claimed for
be tolerant
tomato
for
Cu,
to
cell lines
(Steffens
example,
which
et
is
on
al.
increased
1986),
obviously
production
of
then Cd-tolerant
not
the rule
(y-EC)„G’s,
plants
&
(Schat
such
should also
Ten Bookum
1992b).
to
According
carrier
system,
Vogeli-Lange
for metal transport
which
means
&
Wagner (1990), (y-EC)
G’s
that their impact will
depend
on
it
would
exist,
their breakdown,
could be masked
which
however, how such
a
presumably
possible
growth
description
et
al.
1992)
inhibition such
of CdS
as
crystallite
makes it
more
a
takes
coated with
to
a
rather than their
turnover rate
(y-EC)
G’s in
be reconciled
G
n
as
easy
the
to
rate
of
imagine
with the above
levels and the
in Cd-treated
Cd-(y-EC)
not
& Kalff
when-
tolerance,
n
(y-EC)„G
vulgaris (Schat
(y-EC)„G’s
consider
can
between
as
buffer
purely cytoplasmic
in the vacuole. It is
turnover
relationship
found in Silene
difficult
a
tolerance-correlated increase in
place
variation in
mentioned tolerance-independent
root
by
as
their
concentration in the cell. This could imply that the role of
ever
should be considered
n
into the vacuole rather than
1992).
tomato
degree
The
of
recent
plants (Reese
metal transporter.
W.
238
Fig.
3. Model of the zinc tolerance mechanism
Organic
acids.
pounds,
e.g.
et
al.
Pelosi
al. 1976; Lee
that Zn-tolerant and Ni-tolerant
It is
compounds.
concentrations,
Vacuoles
et
al.
both
after Ernst
proposed
citric
et
1975
and
play
to
al.
a
role
H. SCHAT
metal-binding
as
in
com-
1977; Godbold
1975; Mathys
hypothesis
AND
Mathys 1975a).
and malic acid
This
1988).
the
case
is based
on
et
the observation
whether this is due to increased
cytosolic
or
vacuolar
(see below).
storage compartments
as
Vacuoles of metal-tolerantplants, but also those of non-tolerant plants after exposure
high
al.
of Ni tolerance
often exhibit increased concentrations of these
plants
uncertain, however,
or
J. A. C. VERKLEIJ
ERNST,
for Zn (Ernst
1989), and malonic,
et
O.
(modified
have been
malic and citric acid
1984; Barmens
(Sasse 1976;
acids
Organic
H.
metal concentration (Mullins
et
al.
1985),
often contain
to a
concentrations of heavy
high
metals, especially ofzinc and nickel (Ernst 1969, 1972a, 1974,1980; Sasse 1976; Brookesct
al.
and
1981)
cadmium
to
&
(1975)
degree
Wagner
and
for Zn transport
detoxifying it,
lesser
1980; Heuillet
(Ernst
Vogeli-Lange
Ernst
a
copper and
al.
et
lead
the
tonoplast.
and the Zn-malate complex
would remain bound
anthocyanidines,
According
G
Cd-(y-EC)
to
Mullins
et
al.
1987; Krotz
1985)
et
al.
the zinc-malate-shuttle hypothesis
Malic acid would bind Zn in the
would be
transported
dissociated in the vacuole, after which malate would be
Vacuolar Zn
1974;
and
1989;
1990).
Mathys (1975a) postulated
over
(Ernst
1986; Rauser & Ackerley
to
retransported
stronger chelators,
such
cytosol, thereby
the
over
tonoplast
into the
citrate,
as
(Fig. 3)
and
cytosol.
oxalate
or
when present.
Vdgeli-Lange
&
Wagner (1990),
In the vacuole
complex.
the
Cd is
transported
complex
will
over
dissociate,
the
tonoplast
dependent
on
as
a
the
n
concentration of and the
the
Cd-(y-EC)„G’s
only
in
affinity
low molecular Cd-(y-EC)
Cd of other
to
chelators,
as
well
as
on
In the absence of other chelators with
question.
G’s will rapidly dissociate
at a
a
the chain length of
high affinity
to
Cd,
normal vacuole pH of about
n
5
(Reese
&
Wagner
1987;
lation of undissociated
Matsumoto
Cd-(y-EC)
et
al.
1990).
At
high
Cd exposure
G’s in the vacuole may be
levels,
unfavourable,
as
accumu-
this would
n
drain
too
much of the
molecular
cytoplasmic pool
of glutathione
(Scheller
sulphur compounds. Therefore, re-transport
amino acids
seems to
be
a
prerequisite for
is known, however, about these processes.
an
of
et
al.
(y-EC) G,
1987),
or
or
of the
other low
composing
n
effective compartmentation of Cd. Nothing
METAL TOLERANCE
Recent
application
information
IN
PLANTS
of
X-ray cryo-microanalytical
the final
on
&
gigantea (Rauser
speciation
Ackerley
1987),
with Cd and S in immature cells
treated cells contain vacuolar
Steveninck
P) (Van
observed after
zinc
of
heavy
sulphate
solutions
et
deposits containing
al.
1987,
zinc chloride, but
(Gries 1965).
indicate that crystals
The
are
an
1990a,b,
al.
et
Zn
provided
cells of
root
In
1990a,b).
phytate (Zn,
contrast
K and P
for 48 h in 0-2
rather than a rule with respect
exception
deposits
Zn-
Cd,
to
or
Zn, Mg,
K
been
solutions of
m
concentrations of water-soluble metals in
high
Agrostis
formation has also
1992). Crystal
vulgaris
some
levels of Cd
high
found after incubationin other metal
not
was
At
but sheet-like
cells,
mature
cells of Silene
incubating epidermal
or
Steveninck
(Van
vacuoles.
first detected in
P,
found in
were
have
techniques
metals in
K and
globular deposits containing Cd,
exposure,
and
239
sulphate
plant
extracts
the form of storage
to
of heavy metals in vacuoles.
It
has often been
that
postulated
tolerance may
be
due
to
increased
an
transport metals into the vacuole. The latter could conceivably rely
centration in
ported
over
affinity
or
tonoplast,
of the
capacity
metal storage
higher
plants, including
in
grown
the
Silene
et
such
vulgaris
zinc
et
al.
1981).
As outlined
concentrations of these
cytosolic
vacuolar metal
compounds
found that both zinc-tolerant and
able
to
zinc
pump
tolerant clones
at
into
the
tolerance would rely
on
a
primary
same
cause
fixed internal zinc
plant Cardaminopsis
be due
to
an
vulgaris,
slightly
to
suggests
that
(1974)
capacity.
by
zinc
(Gregory
(J.A.C.
rather
be
to
they
the
plants
exhibit
1976;
shown whether the
broke
necessarily
not
well
as
Deschampsia
mechanism
are
Mathys
1976; Sasse
They might
consequence of metal
a
flux
com-
serve
as
analysis,
cespitosa
were
down
non-
in
that
however,
mean,
that
means
mortality
not
mean,
is
an
increased
example,
& Bradshaw
which is
&
Verkleij
than
a
mere
1965;
P.
in
of
saturation
difficult
to
et
1976),
1992b),
al.
data).
are
and
This
only
whereas
1976),
is
non-
strongly
transport systems
the concentration of
re-
acids with
Agrostis capillaris
(Pelosi
the
a
organic
(Ernst 1975,
unpublished
in
of
tolerance would
it is
general,
production
Zn-tolerant
specific changes
increase
that
Schat & Ten Bookum
Pancaro,
as
the
at
Zn-hyperaccumulating
course,
rich in malate
very
always
occurs
consequence
In
storage capacity.
of
a
of
rather than
strain,
mortality
the Zn-tolerant and
This does
these tolerances involve
tonoplast itself,
as
of tolerances. For
Alyssum hertolonii,
tolerant
that
which both exhibit increased malate levels
Ni tolerant
Ni-tolerant
al.
et
a
1975;
also increased and whether these
tonoplast.
observed that leaf
halleri, suggesting
nature
al.
et
Ni-tolerant
(Pelosi
(c)
that zinc-tolerant
(1981), using compartmental
but
concentration in
increase of the vacuolar
metal-specific
Silene
al.
Ernst
trans-
higher
a
and
itself,
to
con-
higher transport capacity. The breakdown of the transport in
concile the idea of tolerance
the
tonoplast
Also
non-tolerant clones of
vacuole,
of strain. Ernst
of the vacuolar storage
are
the
over
et
non-tolerant clones
also be taken
may
a
be
can
acid, (b)
importance
it remains
exposure levels. This does
higher
the
1976;
1984).
earlier, however,
Brookes
sequestrants.
al.
et
1975,
malonate or citrate
mediate metal transport
pounds really
(Ernst
Godbold
1981;
malic
ability
higher
also exhibit increased malate concentrations if
increased concentrations of malate,
Brooks
in
a
which
complexes
in the vacuole. It may be of
of excessive
al.
metal
forming
(y-EC)„G’s and, possibly,
as
metal-transporting system
capacity
absence
Brookes
1975a,b;
of substances
the cytosol
the
(a)
on
in
the
chelating organic
acids.
In summary,
tolerance
to
although
metals,
of which tolerant
at
it is
likely
least in the
plants
could
that vacuolar
case
of Zn and
accomplish
a more
compartmentation plays
Ni,
the
precise
a
role in the
mechanisms
effective vacuolar
by
means
compartmentation
240
are
W.
completely
unknown. Studies
non-tolerantplants may
provide
J. A. C. VERKLEIJ AND
conceivable that
THE
compartmentation
contribute
can
tolerance
to
WHOLE
PLANT
the whole
and shoot have been
over root
Increased retention in the
it
could be of
uncertain.
a mere
of whether it is
Regardless
plants
if shoots
adaptive
storage).
It has
al.
not a
operating
Wu
1972b;
al.
el
(Baker 1981),
than
in the
root
but
is
which
roots,
not, retention in the root
or
will be
in the distribution
rule
been proven that tolerance involves
never
possibilities
Ernst
sensitive
more
is
1984; Verkleij & Prast 1989).
certainly
are
consequence of the tolerance mechanism
vacuolar
is
el
it
plant,
level of tissues and
plants
frequently reported (e.g.
in tolerant
roots
significance
adaptive
tolerant
a
the
at
level. Several
plant
1975; Baker 1978; Coughtrey & Martin 1978; Lolkema
LEVEL
and cell of
discussed below. Differences between tolerant and non-tolerant
of metals
SCHAT
of tolerant and
tonoplasts
taking place
processes
at
and
H.
insight.
tolerance is apparent in any organ, tissue
Although
organs
AT
ERNST,
isolated vacuoles
on
more
COMPARTMENTATION
H. O.
might represent
cells
increased
(e.g.
genetic changes
other
than those involved in the tolerance mechanism present in every cell.
Transport
of
heavy
metals from root
and Zn; Graham 1981 for Cu, but
et
1988 for Cu,
al.
tolerant
plants
complexes (H.
Pb and
of
Silene
Harmens, pers.
of
potential advantage
removing
exposed
plants
comm.),
In
1990).
contrast
especially during
of leaffall
as
to
Ca,
plant
which
the last week
means
environment and its
of
exhibit
special adaptations
Reproductive
Due
to
the
shown
but
at
metals into leaves is that it
the
highest
to
response
to
compare
through
in the natural
shedding.
with
gradually
their metal burden. Due
throughout
this
the
soils,
year.
of
1984,
1982,
accumulates
use
of Pb in the
senescent
It is unknown whether tolerant plants
not
exhibit
1982;
et
do
organs
production.
e.g. Armeria muelleri,
or
&
in
high
Plants
Mulcahy 1985a,b),
laboratory (Searcy
due
&
to
the
levels of
on
Thlaspi coerulescens.
metals
pollen selection,
been demonstrated in the
at
to
Therefore
heavy
Silene
metal-enriched nutrient solution,
the metal concentrations in all
ones,
survive
In metal-tolerant plants
lower than in
vegetative
not
experimentally.
reproductive
decreased seed
a
environment,
Ernst
plants
nor
reproductive parts. Although
has
Zn
mobility
of tolerant and non-tolerantplants.
cycle
(Searcy
pistils
(Ernst
ageing,
the low
to
non-tolerant
metal accumulation in
the life
Mimulus guttatus and Silene diocia
are
possibility
leaves of metal-
point (see above).
1990),
from the
the
shedding (Fig. 4), suggesting that plants make
al.
vulgaris (Ernst
parts
creates
The oldest
metal concentrations
accumulates
of metal-enriched
metal-enriched soils do
growing
metal
organs
toxicity
impossible
metal
of
differences between free and
plant-internal transport.
reproductive phase in such environments, neither naturally
it is
differences
qualitative
quantitative
accumulation in the roots, the concentration of Pb in
leaves remains about constant
partially
exudates of non-tolerant and metal-
xylem
not
via natural leaf
prior
reducing
high
is mediated at least
leafage
exhibit
generally
of
have
allocating
metals from the
xylem
Van Goor & Wiersma 1976 for Mn
Mn; White etal. 1981 a,b for Cd, Ni and Zn; Mench
not
vulgaris
Allocation pattern of metals and
A
shoot via the
Zn). Analyses
metal ions may affect the
complexed
to
1970 for Mn and Fe;
by organic complexes (Hofner
are not
e.g.
excluded
reproductive plant
metal accumulation in the
Mulcahy 1985a,b,c). Also,
a
METAL
Fig.
TOLERANCE
4. Concentration
lanceolata.
of
some
from Ernst
Data
241
IN PLANTS
mineral
(1984)
elements
and
in relation
to leaf
initiation
in Zn-tolerant
plants
reduction in the percentage of viable pollen in metal-tolerant plants after metal
has been observed
processes
play
a
(Searcy
&
Mulcahy
1985b).
It is unknown,
plants,
seeds have
a
lower metal concentration than any other
part (Ernst 1974, 1982). The concentration in the
embryo,
which suggests that the
location. The low metal concentration of the
extra
THE
testa
is often
two
placenta represents
embryo
may
be
a
to
four times
barrier
to
advantageous
metal
since it
plant
higher
trans-
creates
and early seedling growth.
storage capacity during germination
COSTS
Selection
METAL TOLERANCE
metal tolerance
1968; Cook
tolerance has
be
OF
against
(McNeilly
may
treatment
whether these
however,
role in the natural environment.
In metal-tolerant
than in the
of Plantago
unpublished.
a cost.
et
al.
In the
case
(partly) explained by
Baumeister
1954; Schat
on
unpolluted
1972; Hickey
an
& Ten
&
of tolerances
apparent
Bookum
soils
McNeilly
to
has
been
1975),
essential
clearly
which
metals,
the
The fact
that metal
of tolerances
costs
increased need for the metals in
1992a,b).
demonstrated
implies
question (e.g.
that tolerant
plants
often
242
W.
exhibit maximum
growth
has been
tolerant,
itself. The reduced uptake,
the
of
activity
concentration,
activity
than non-tolerant
lower
as a
tolerant
consequence
growth
have been observed for Zn
non-essential
metals,
Even when grown
too
(Baker
the
at
has been
growth
mum
might
It
and
1954). Only
levels.
in
1975a,b),
for
1989,
ones
well represent,
as
a
Cu
al.
et
certain
more
interpretation
of these
zinc
1975;
maximum
(Lolkema
et
experiments,
al.
some
survey).
a
clones
or
usually
This difference in maxi-
1988).
of the tolerance mechanism
cost
of adaptation
consequence
environ-
to
mental conditions other than the elevated metal availability itself, e.g. the nutrient
of the soil. A
a
concen-
optimum
activity (Ernst
1976),
exter-
consequence,
shift in the
a
(Sasse
the energy
however,
are
carboanhydrase
a
increased zinc
in short-term
Wilson
(Ernst 1983;
they
low
at a
metal demand for
the
Ni
as
metal concentration, tolerant plants
tentatively explained
as
compared
at an
Such
which
to
50% lower
nitrate reductase
although only
& Walker
optimum
a
SCHAT
of the metal would reduce
1975a,b), and, possibly
activity
(Mathys
1992a,b),
non-tolerant
grow slower than
(Ernst 1983).
exhibits
Tolerance-correlated increases
1975a,b).
Schat & Ten Bookum
1984;
operation
H.
of the tolerance mechanism
sequestration
(Baumeister
too
concentration has also been observed for
Mathys
of the
vulgaris
plants (Mathys
reach normal
plants
A. C. VERKLEIJ AND
metal-stimulatedenzymes. If
or
Zn-tolerant Silene
photosynthetic activity
tration,
J.
ERNST,
increased cellular
or
metallo-enzymes
nal zinc
O.
elevated, normally toxic levels of the metal
at
explained
H.
phenomena
requires
a
status
genetic analysis.
REFERENCES
Antonovics,
J.
The
(1966);
and
genetics
evolution
of
Bradshaw,
differences between closelyadjacentplantpopulations
in
with
Rozema
special references
PhD.
Thesis, University
C.J.
Asher,
by
&
barley
J.
Plant
uptake
Physiol.
6:
459-466.
(1978): Ecophysiological
aspects
Silene maritima With. New
zinc tolerance in
of
Phytol.
80: 635-642.
Baker,
to
Walker,
and
Bioavailability 1:
M..
plants
and
to
excludersmetals.
heavy
66: 438
bei Silene
W.
(1989): Physiological
and the
quantification
Chem.
toxicity.
Speciation
E. &
of
a
Price,
C.A.
cadmium
(1980):
Partial
binding protein
of a cadmium-treated tomato. Plant
from the roots
Baumeister,
P.L.
7-17.
Breman,
characterization
Physiol.
441.
(1954): Ober
inflata Smith
den
Einfluss
des Zinks
I. Ber. Deulsch. Bol. Ges. 67:
205-213.
logical role
of zinc in
biomembranes.
resistant
1098.
A. D.
to
Life
the
(1987): A
structure and
Sci. 28:
and
zinc
physio-
function
of
1425-1438.
(1952): Populations
lead
critical
of
poisoning.
Nature
169:
Stresses
2-5.
Kluwer
Untersu-
(1962): Genelisch-physiologische
Sm.
Inaugural-Dissertation
Munster.
J.C. &
Thurman,
DA.
(1981):
of zinc tolerance in grasses.
J. Plant
Nutr. 3: 695-705.
Shaw, S.
chemical
nickel
in
some
Plant. 51:
Butler,
form
M.
& Asensi
and
Iberian
A.E.J. &
vulgaris.
Plant Cell Environ. 3:
Cakmak, J. & Horst,
in
H.
and
permeability
plants.
D.A.,
the
Young,
tolerance
Plant
&
of
Physiol.
J. Plant
in
T.R.
Physiol.
H.,
&
Wildering,
in intact
zinc
R E.
soybean
(1975): Absorption du
(Zea
mais
L.)
cuivre
et de tournesol
Plant Soil 42: 65-83,
Assche,
Physiological responses
tamination with
of
73: 844-848.
L.
de mais
Van
in membrane
roots
132: 356-361.
Physiol.
Garland,
(1980):
Chlorella
119-126.
(1988): Increase
exudation
Salsac,
par les racines
Clijsters,
(1981):
M.M.
alga
green
(1983); Cadmium uptake kinetics
Cathala, N.
A.
function
Alyssum species.
Copper
Cataldo,
Marfil,
physiological
167-170.
Haskew,
(Helianthus annuusL.).
Agroslis tenuis
In;
(eds): Ecological
,
Brooks, R.R.,
plants.
B.L.
J.A.C.
Environmental
to
Stress tolerance
framework.
Publishers, Dordrecht.
Universitat
deficient
Bettger, W.J, & O’Dell,
Bradshaw,
Verkleij
Brookes, A., Collins,
The
metals
heavy
tolerance
Bartolf.
of
response
Nutr. 3: 643-654.
responses
of
Accumulators
(1981):
in the
A.J.M. &
Baker,
W.
Broker,
(1991):
evolutionary
and
The mechanism
A.J.M.
strategies
J. Plant
Academic
T.
McNeilly.
chungen in Sileneinflata
A.J.M.
Baker,
J.
Responses
Arsenic
(1979):
Auslr.
seedlings.
tolerance.
of Wales.
P.F.
Reay,
metal
heavy
to
A.D..
plants—the
of
F.&
Gora,
higher plants
L.
(1991);
to soil con-
metals. In: Rozema J. and
Verkleij
METAL TOLERANCE
J.A.C.
IN
PLANTS
to Environmental
(eds): Ecological Responses
Stresses.
32-39.
Kluwer
243
Academic
Publishers,
De
Dordrecht.
Cook,
S.C.A.,
C.
Lefebre,
between
Competition
plant populations
&
tolerant
metal
normal
on
T.
McNeilly,
soil.
(1972):
normal
and
Evolution
26:
366-372.
D.A. &
Uptake patterns
of free and
in
of
excised roots
Z.
Zephyr).
uptake and
(1977):
ions
barley (Hordeum vulgare
L.
cv
&
Martin,
M.H.
Cadmium
(1978):
lantus L.
Holcus
grown in
solution
Oikos 30: 555-560.
of
properties
of
the
soluble
zinc-tolerant
Anthoxanthum
M.
Brett,
acid
and
(1976): Some
phosphatases
non-tolerant
odoratum.
New
of
clones
7:
Phytol.
R.M. &
Thurman, D.A. (1978): Inhibition by
of soluble
and cell
wall
acid
G.C.
Phytol.
80:
metal tolerance in grasses.
of Anthoxanthum
of
of cellular
Rapidity
Trans.
Rhod. Sci. Assoc.
'
D.
zinc-tolerant
and
Phytol
M.S. &
differences
odoratum
10: 47
Z.
De
T.
L.F,
on
of the
Kluwer
M.S. &
Anthoxanthum
to aluminium.
Francis,
D.
The
effect
of
cells
14: 399^106.
metal
heavy
of Chlorella
cells.
92: 39^19.
in
gold mine.
Verkleij
J.A.C.
Publishers,
Datura innoxia and
Physiol.
Tomsett,
sediment
North
and
Portugal.
(eds): Ecological
Stresses,
42—47.
Dordrecht.
L.D. &
Robinson,
binding with
syn-
cadmium.
89: 700-706.
A.B.
(1990):
flowering plant
Vos,
and
C.H.
free
De
Vos,
C.H.R.,
W.H.O.
cell
root
plasma-
cucubalus.
Physiol.
De
R.,
Vooijs,
in roots
Metallothionein
D.A. &
genes
from
Mimulus guttatus. FEBS Letters
Glutathione
induced
in
roots
of
stress
copper tolerant
the
J.
phytochelatin
in
R. &
due
depletion
synthesis
Silene cucubalus.
copperoxi-
causes
Plant
H.
Schat,
to
Physiol
98:
metals
and
853-858.
Dueck, Th.A., (1986): Impact of heavy
air
pollutants
on
Doctoral
plants.
Thesis,
Vrije
Universiteit, Amsterdam.
metal
(1984): Heavy
of
emission
Angw.
sources.
(1986):
Vesicular
zinc-toxicity
to
Duvigneaud,
de
arbuscular
P.
&
Pasman, F.
genetic
consti-
vicinity
of two
Bot. 58:47-59.
W.H.O. &
in
H.
Schat,
mycorrhizae
decrease
zinc-polluted
18: 331-333,
La
(1958).
the
growing
grasses
sol metalliferes.
ses
and
in
plant populations
metal emission
vegetation
Bull.
Soc.
du
Katanga
Bot.
r.
Betg.
et
90:
127-286.
suchungen
den
in
unter Einschluss
Inaugural-Dissertation Universitat
Ernst,
W.H.O.
Der
(1968):
die
Einfluss
Wirkung
Plant.
Ernst,
einiger
der
Alpen.
Munster.
der
Phosphatver-
ionogenem
von
chelatisiertem Zink aufdie Zink- und
nahme
Unter-
Schwermetall-Pflanzengesell-
schaften Mitleleuropas
und
Phosphatauf-
Schwermetallpflanzen.
Physiol.
21:323-333.
W.H.O.
Zur
(1969):
der
Physiologic
Schwer-
raetallpflanzen—SubzellulareSpeicherungsortedes
Ernst,
W.H.O.
heavy
8:
metal
161-164.
(1972a): Ecophysiological
plants
in
studies
on
South Central Africa. Kirkia
125-145.
Ernst,
W.H.O.
Schwermetallresistenz
(1972b):
Mineralstoffhaushalt.
Nordrhein-
Land.
Forschungsber.
2251:
Westfalen
1-38.
Westdeutscher
Verlag, Opladen.
Ernst,
Z.
W.H.O. &
Weinert,
Zink in der Blattern
H.
von
(1972):
Silene
Lokalisation
cucubalus
Wib.
Pflanzenphysiol. 66:258-264.
Ernst, W.H.O.,
Mathys,
W. &
Janiesch,
P.
(1975):
Physiologische Grundlagen der Schwermetallresistenz.
damage
Ernst,
to
of Silene cucubalus.
Vos, C.H.R., Vonk, M.J., Vooijs,
von
(1991): Copper-induced oxidative
radical
&
135: 165-169.
Physiol
(1992):
H.
Schat,
(1989): Copper-induced damage
permeability barrier
und
260: 277-280.
De
the
copper-tolerant Silene
Zinks. Ber. Deutsch. Bot. Ges. 82:
water,
Environmental
to
J.
(1991b):
Miranda, J.R., Thomas, M.A.,Thurman,
the
Exper-
(1989): Poly(Y-glutamyl-cysteinyl) glycine
Plant
De
of
permeability
dales
Academic
thesis in
lemma in
resistance to
Ernst, W.H.O. (1964): Okologisch-soziologische
(1973): Physiological
Delhaize, E., Jackson, P.J., Lujan,
NT.
of
copper-induced damage
sorgung sowie
Arsenic
In: Rozema J. and
Responses
R.W.
Response
(1979):
the
(1991):
vegetation
of Festuca
from the Park Grass
II.
a
103-108.
Plant Cell Environ.
Pflanzenphysiol.
Koe,
cultivar
in
vacuolation in root meristematic
of Festuca rubra L.
Filippis,
(1991a):
zinc
by
55.
R.L., Davies,
compounds
J.D.
induced
populations
among
Zinc-induced
De
117:
Snaydon,
Rothamsted.
Davies,
Thomas,
non-tolerant
L. collected
Ecol.
&
changes
rubra L. New
Appl.
Thesis,
Vooijs,
Increased
(1991):
soil. Soil Biol Biochem.
Davies, M.S., Francis,
iment
W.H.O.
Dueck, Th.A., Visser, P., Ernst,
measuring heavy
58:9-16.
Davies,
Ernst,
tution
17-32.
A method
(1977):
zinc
of zinc-
phosphatases
and non-tolerant clones
odoratum. New
Craig,
Doctoral
Dueck, Th.A., Ernst, W.H.O., Faber, J.
547-552.
tolerant
cucubalus.
Vos, C.H.R., Schat, H„ De Waal,
R. &
dative stress
D.A. &
Cox, M.R., Thurman,
Cox,
Silene
Universiteit Amsterdam.
Plant
distribution in tolerant and non-tolerant
populations of
of
N.W.
Lepp,
complexed copper
Pflanzenphysiol. 82:435-439.
P.J.
Coughtrey,
roots
sensitive
Plant 82: 523-528.
Coombes, A.J., Phipps,
culture.
and
Vrije
Enzymaktivitaten
Forschungsber.
Land.
1-38. Westdeutscher
und
organische
Nordrhein
Sauren.
Westfalen.
Verlag, Opladen,
2469:
244
W.
W H O.
Ernst,
(1974):
Erde. G. Fischer
Ernst,
W.H.O.
resistance
in
W.H.O.
Ernst,
Effects
(1975):
Ini.
W.H.O.
mium
in
plants.
New
in
Press,
Nriagu
I,
639-653.
(ed.)
115-133.
Plants,
aspects of cadCadmium
(ed.)
John
&
Wiley
in
Sons,
York.
Ernst,
Kinzel
H.
(1982):
W.H.O.
Ernst,
Schwermetallpflanzen.
In:
(ed.) Pflanzenokologie und Mineralstoff-
472-506.
wechsel,
strategien
Ulmer
(1983):
Okologische
Bodenfaktoren.
an
W H O.
lanceolala.
AnpassungsDeulsch.
Ber.
sampling.
Element
Bol.
Lieth
W H
chelatins
impact on
in
(re)-
representa-
and Markert
H.
H. &
Verkleij,
of metal
Evol. Trends Plants.
Ernst, W.H.O. &
be
Verkleij,
used
for
In; Farmer
ability?
Environment
B.
(eds);
ecosystems,
P.M.,
resistance
J.A.C.
in
Silene
Can
phyto-
of metal
1:
(Edinburgh 1991)
avail-
Metals in the
111114.
CEP
N.J.
from
(Pisum
sativum
to
metallothionein
genes.
29
32.
Farago,
late
&
Greg,
J.
Pitt,
R.R.D.
(1977):
metals. Part 111. A
Australian
A
(1990):
with
L.)
FEBS
J.A.,
gene
homology
266:
Letters
species
Plants which
further
accumu-
investigation of
which take up zinc.
Inorg.
two
Chim.
Acta. 24:211-214.
&
zinc and
organic
non-tolerant
Plant
R .D.
In:
roots.
Graham
141
Accumulation
of Deschampsia
of
and
caespilosa.
J.
116: 59-69.
Goneragan
A.D.
Press,
PhD. Thesis
R.P.G.
J.F.,
(eds): Copper
(1965):
&
in
bei
und
Galmeiokotypen
Silene
von
cucubalus
Wib.
Flora
& Ernst, W.H.O.
in
the
L.
Agrostis capillaris
(1990):
metal
heavy
The role of
tolerance
of
Environ.
Agric. Ecosyst.
29:
173-177.
E.,
E.L.
Winnacker,
the
(1985a): Phytochelalins:
of
complexing peptides
&
M.H.
Zenk,
principal heavy-metal
higher plants.
Science 230:
E.,
Grill,
E.G.
Winnacker,
Phytochelatins,
from
a
class of
plants,
metallothioneins.
&
M.H.
Zenk,
(1987):
heavy-metal binding
pep-
functionally analogous
are
Proc.
Nall.
Acad.
Sci.
to
84:
USA
E..
Grill,
M.H. &
Zenk,
Induction
of
chelatin
cadmium
by
Winnacker,
heavy
in
cultures
cell
serpentina. Nalurwissenschaften
S.C. &
E.L.
(1985b):
metal-sequestering phyto-
P. B.
Goldsbrough.
of
Rauvolfia
72:432-433.
(1991): Phytochela-
tin accumulation and cadmium tolerance in selected
tomato cell
lines.
K.
Physiol.
Plant
permeabilities through lipid
Biochim.
Hall,
Biophys.,
A.,
Mechanism
AH.
of
Ernst,
H.,
Silene
in
1989),
2:
Harrison,
J.A.C.,
=
for
an
195-199.
Koevoets,
cucubalus).
Silene
&
P.
In:
copper
Vernet
(Geneva
Consultant, Edinburgh.
178-181. CEP
desorption
Biol. 54:
Metals in the Environment
S.L., Lepp,
of
(1979):
the mechanisms of zinc tolerance
vulgaris (
(ed.): Heavy
M.
Bulter,
The role of organic acids and
(1989):
phytochelatins
ion
membranes.
185-188.
&
Mar.
Verkleij,
W H O.
thallous
siliculosus- —Evidence
mechanism.
Harmens,
and
bilayer
tolerance in the marine foul-
copper
alga Eclocarpus
exclusion
J.P.
Act 735:
Fielding,
97: 306-312.
Cadmium
(1983);
N.W, &
from the free
N.A.
Phipps,
excised
by
II,
roots.
space. Z.
(1979):
Copper
Pflanzenphysio!.
94: 27-34.
Hassen,
zinc
M M,
&
uptake by
Tang
Han
Hai
citrus roots.
Z.
(1976):
Kinetics
Pflanzenphysio!.
of
79:
177-181.
of copper
(1981): Absorption
R.P.G.
grasses.
Gregory,
(1984):
acids in roots of zinc tolerant
163. Academic
Gregory,
H.
ecotypes
Physiol.
Graham,
W.J., Collins, J.C., Thurman,
Marschner,
Inaugural-
Munster.
Zinkresistenz
mycorrhiza
Uptake
D.L., Horst,
Godbold,
D.A.
VA
in
M.E. &
Universilat
and
Galmeiokotypen
cucubalus.
BI56:271-290.
ing
Gatehouse,
L.N.,
Robinson,
pea
die
Gutknecht,
(1991):
(ed.): Heavy
Gatehouse.
an
Silene
von
(1966): Zellphysiologische Untersuchungen
Normalformen
Gupta,
(1990):
4,45-51.
estimation
J.G.
J.A.C.
Consultant, Edinburgh.
Evans,
liber
SCHAT
439-443.
and
Verlagsgesellschaft, Weinheim.
O., Schat,
Evolutionary biology
vulgaris.
Plantago
allocation
cadasters
concentration
17-40. VCH
Ernst.
in
15-19.
and its
plants
In:
tolerance
Element
(1990):
translocation in
tive
Metal
Nieuwsbrief
W.H.O.
Ernst,
Dissertation
B,
H.
(1965): Zellphysiologische Untersuchungen
Normalform
tides
(1984):
VERKLEIJ AND
674-676.
Verlag, Stuttgart.
Ges. 96:49-71.
Ernst,
der
Grill,
W.H.O.
C.
Griffioen, W.A.J.
Cambridge.
J.O.
B.
Gries,
Gries,
and biochemical
Biochemical
In:
Environment
the
Metals in the
In: Mansfield T.A.
Pollutants
(1980):
metal
heavy
121-136.
pp.
(1976): Physiological
Cambridge University
Ernst,
of
Conf. Heavy
1975.
J. A.
ERNST,
iiber die Resistenz gegen Zink
Physiology
Toronto
Air
of
der
Schwermetallvegetation
of metal tolerance.
aspects
O.
Verlag Stuttgart.
plants.
Environment,
H.
Robson
in
Soils
by plant
A.D.
and
and
Plants,
metal
University
Bradshaw,
metal
tolerance
Sibth.
and other grasses. New
populations
tolerance
in
of Wales.
A.D.
of
Moreau,
thiole-molecular
Agrostis
Phytol.
64:
tenuis
131-143.
A..
Halpern, S.,
Cadmium
(1986):
in vacuoles
with Cd
Jeanne,
binding
of Dunaliella
Cl,: electron
N,,
to
a
bioculata
probe analysis.
Biol Cell 58: 79-86.
Hickey,
(1965): Heavy
S.
Puiseux-Dao,
contaminated
Sydney.
Heavy
E.,
Heuillet,
D A.
between
lations:
&
McNeilly,
metal
a
field
29:458-464.
tolerant
T.
and
(1975): Competition
normal
experiment on normal
plant
popu-
soil. Evolution
METAL TOLERANCE
Hille, B. (1984):
Sinauer
Ionic channels
PLANTS
ofexcitable
dungen
im
Physiol.
Plant.
tolerance to
(A.
Helianthus
annum.
M.K,
Relation-
(1984):
metals in
heavy
Agroslis
Phytol.
New
98:
177-190.
W.A.J. &
of
Agrostis
without
or
Ernst,
W.H.O.
of VAM infection in three popu-
(1992); Seasonality
with
capillaris (Gramineae)
soil
on
metal enrichments. Plant Soil
heavy
139: 67-73.
to
Mechanism of trace
(1990):
In: Katterman
plants.
Plants,
Jellinek,
metal
F.
(ed.);
231-255. Academic
H.H.G. &
Sangal,
ions
water
from
metal tolerance in
Environment
San
Press,
S.P.
Injury
Diego.
D.
Collection
(1972):
by polygalacturonic
of
acids.
(1958):
of
Populations
Agroslis
ssp,
tolerant of heavy metals. Nature 182: 816-817.
Jowett,
in
D.
(1959): Genecology of heavy
Agroslis
action
Ph D. Thesis
spp.
C.D.
Kennedy,
&
the trans-root
on
excised roots. J.
exp.
and
S.D..
toxicity
Martin,
effects
S.H,
Sanders,
the
and
+
efflux of
Wagner,
G.J.
(1989):
cadmium, zinc, Cd-peptide,
tobacco
suspension
cells.
Plant
(1978):
of
Lead
acid induced cell
simulation
S.P.
McGarth,
of complexation
iron,
1. Effect of EDTA
R.,
manganese,
in
a
J.
study.
nickel
Brooks,
between
Ernst,
R.R.
copper
multi-metal
and
Bol.
42:
exp.
&Jaffre,T.(1978):
nickel
(1985): Copper
P.C.,
and
citric
resistance
Thesis,
W.H.O.
acid
in
Vrije
in
higher
Universiteit
M.H.,
The
(1984):
in
Silene
Schouten,
possible
cucubalus.
A.J.
role
Planta
&
of
162:
Vooijs,
in Silene cucubalus.
per and
its effects
synthesis.
anderen
The
copper
Mimulus
flower,
50: 283-293.
M.
Werff,
&
92:
uptake by
Elodea
leaves
Z.
nuttallii.
1-10.
(1975a):
bei
W.H.O.
Ernst,
and zinc
copper
aquatic plant.
an
Arten.
control of
genetic
yellow monkey
der
Zinktoleranz
W.
Mathys,
resistant
Physiologische
Silene
der
Aspekte
cucubalus
Wib.
und
Universitat
Inaugural-dissertation,
(1975b):
and
and
metals
vitro
in
their
of
Enzymes
non-resistant
cucubalus
W.
Mathys,
mustard
in
heavy-metal-
populations
interaction
and
vivo.
The role
(1977):
oil
with
of Silene
heavy
some
Plant.
33:
malate, oxalate,
and
Physiol.
of
in
glucosides
the
evolution
of zinc-
Plant.
40:
Matsumoto, Y,, Okado, Y., Min, K.S., Onosaka,
S. &
resistance
in
herbage plants. Physiol.
130^136.
K.
XXVII.
Amino
(1990):
of their
Chem. Pharm. Bull.
D.C.H. &
and
peptides.
metal-binding properties.
38: 2364-2368.
R.A.
Hassall,
Chlorella
potassium by
acids
of phytochelatin-related peptides
Synthesis
and examination
toxic amounts of
T.S.
in
(1965):
Loss of cell
after contact
vulgaris
copper
with
Plant.
sulphate. Physiol.
T.
of
copper toler-
Ph.D.
(Sibth.).
Evolution
(1968);
populations.
111.
Thesis,
A.A. &
phosphate
Macnair,
uptake
Holcus lanatus
A.A.
closely adjacent
on a
small
copper
An
altered
(1990):
in
Phytol.
Macnair,
and
M.R.
system
L. New
&
accumulation
in
tenuis
Argostis
23:99-108.
Heredity
Meharg,
tenuis
of Wales.
University
McNeilly,
The evolution
(1965):
Agrostis
Holcus
arsenate-tolerant
116: 29-35.
M.R.
translocation
ant and non-tolerant
Meharg,
A.A.
mechanism
cespitosa
Planla
R.
(1986): Copper
Subcellular
on
chloroplasts
167: 30-36.
tolerance
distribution of copand
plastocyanin
Phytol.
&
Macnair,
of arsenate
Beauv.
(L.)
Adaptation
174-179.
P.C. &
to
L.M.
Cook
(1991a):
in
Uptake,
arsenate
lanatus L. New
toler-
Phytol.
117: 225-231.
Donker,
metallothioneins
Lolkema,
the
of
W.
Mathys,
ance
Amsterdam.
Lolkema,
and roots
Meharg,
Doctoral
plants.
in
Kinetics of
(1979):
on
accumulating plants. Phytochemistry
P.C.
higher plants
and
London.
Press,
(1983):
Heredity
gullalus.
McNeilly,
17: 1033-1035.
Lolkema,
M.R.
Marquenie-van
mine.
relationship
some
199. Academic
&
500-513.
Lee, J.R., Reeves,
of
J.M.
Bishop
18: 1053-1065.
N.P.,
Influence
(1991).
uptake by plants
zinc.
J.F.
Garrod,
ofindole-3yl acetic
Tancock,
J.R.
computer
The
137
Macnair,
Mcßrien,
E.S. &
209.
Tolerance
In:
higher plants.
(eds): Genetic Consequences of Man-Made Changes,
Tanaka,
Planla 144: 79-84.
elongation.
Laurie,
H
copper
91: 780-787.
Physiol.
Lane,
acid in
organic
The
(1987):
38: 800-817.
B.P. &
between
of Wales.
mercury,
potential and
Bol.
Krotz, R.M., Evangelun,
Relationships
F.A.N.
zinc, cadmium,
197
(1981):
Patch-
(1991):
of
161-165.
metal tolerance
University
Gonsalves,
of divalent
and lead
40:
H.B.A,
membranes
Munster.
Water Res. 6: 305-307.
Jowett,
cell
Pflanzenphysiol.
Jackson, P.J., Unkefer, P.J., Delhaize, E., Robinson,
N.J.
M.L.
Prins,
&
in
Acta 801. Need.
Macnair,
tolerance
letswaart, J.H., Griffioen,
lations
F.J.M.
studies
toxic materials.
Sibth.).
tenuis
Maathuis,
clamp
23: 673-677.
between
L.
membranes.
manganhaltigeVerbin-
von
M.D. & Nicolls,
Humphreys,
capillaris
Eisen- und
Blutungssaft
245
MA.
Associates, Sunderland,
Hofner, W. (1970):
ships
IN
of
the
M.R.
tolerance
and
arsenate
Agrostis
The
Deschampsia
capillaris
uptake system.
L
New
119: 291-297.
Mench, M„ Morel, J.L., Cuckert,
(1988):
(1991b):
in
Metal
molecular
binding
weight.
with
root
A.
&
Guillet,
exudates
J. Soil Sci. 33: 521-527.
B.
of low
246
W.
Mukherji, S.
olism
of
&
influenced
toxic
by
Pflanzen. Physiol.
Mullins,
(1977): Growth
metal
concentrations
of
K. & Thurman.
location
in
microscopy
L.)
seeds
lead.
by
D.A.
Z.
fixed
conventionally
(1985):
electron
analytical
and
freeze-
the
In:
Lekkas
Environment
Consultants
T.D.
in
CEP
&
Biochem.
Y.
Hayashi,
(1981): Purifi-
in UV and CD
unique properties
Schizosaccharomyces
Res.
Biophys.
103:
Commun.
10211028.
R.A.A.
M.K. &
and
Sibth. New
P.
Nissen,
tolerance
T.
to copper in
Agrostis
tenuis
83: 653-664.
and
cations, chloride,
plants.
boric acid.
II.
Physiol.
Plant. 29: 298-354.
Pelosi, P., Fiorentini,
nature of nickel
Desv.
Agric.
P.J.
Peterson,
exp.
Bol.
The
(1969);
in
distribution
zinc
I.L.
(1969):
Peterson,
by plants
tissues. J.
lead
and
odoratum
Mechanism
for
antipyretica.
P.J.
mine
on
(1975): Arsenic
(United Kingdom).
waste
4: 365-371.
Hardwick,
zinc
tolerance
in
Anthoxanthum
Davies,
The influence
of
of
M.S.
of zinc
a
on
&
the cell
zinc-tolerant
Festuca
rubra
cycle
and
L.
Davies,
Effects ofzinc
on
a
RNA and
on
cell,
protein
zinc-tolerant
M.S. &
a
Powell,
M.J., Davies,
Effects
root
of zinc
hairs
and
102;
xylem
Prat.
S.
and
size,
cultivar
of
Francis,
size
and
to the
elements
non-tolerant
Ber.
Die
Erblichkeit
D.
(1986c):
proximity
root
tip
in
of
a
cultivar of Festuca
in
J.
of
Plant
C.A.
granules
of
differentiating and
J. Bol. 65:643-646.
Can.
roots
Localization
(1987):
within
(1980): Metallothionein
to
tolerant
Agrostis
copper.
Nature 287: 563-564.
R.N.
tobacco
&
Wagner,
(Nicotiana
G.J.
(1987): Properties
tabacum)
of
cadmium-binding
Biochem. J. 241: 641-647.
peptide(s).
R.N,
White,
C.A.
&
D.R.
Winge,
(1992):
Cadmium-sulfidecrystallitesinCd-(y-EC)„G peptide
from tomato. Plant
complexes
C.
(1967):
Zambian
Reilly,
C.
homblei
98:225-229.
Physiol.
Accumulation
plants.
Rowel,
of
by
copper
some
Nature 215: 667-668.
J. &
J.
Stone,
binding ofcopper
(De Wild.) Duvign.
(1970);
The
accumu-
in leaf tissue of Becium
& Plancke.
New
Phytol.
des
Proto-
69:993-997.
G.
Die
(1963):
hoherer
plasmas
Proloplasma 57:
N.J. &
metal
Kupferresistenz
Pflanzen
N.J.
&
auf
anism
of
copper
F.
(1966):
(1986):
complex in
in
B227:493
their
Plant. 67:499-506.
D.A.
tolerance
R. Soc. London
angiosperms;
Physiol.
Thurman,
Metallothio-
(1986):
in
complexes
ment of a metallothionein-like
Proc.
Kupfererzbdden.
643-659.
Jackson, P.J.
structure and function.
Involve-
the mech-
Mimulus
guttatus.
501.
Vergleichende
physiologische
Resistenz
Deulsch. Bol. Ges. !52: 65-67.
gegen
iiber die Zinkresistenz
Schwer-
von
Munster.
F.
Riither,
(1967):
Vergleichende
Untersuchungen
iiber
die
physiolo-
Resistenz
Schwermetallpflanzen. Protoplasma
A.K.
(1989): Copper phytochelatins
Land.
guttatus. Proc. R. Soc.
der
Serpentinvegetation
in
Osterreich und Deutschland.
&
of
Sewell,
Mimulus
236: 79-89.
(1976): Okophysiologische
F.
von
64:400-425.
Salt, D.E., Thurman, D.A., Tomsett, A.B.
Unlersuchungen
Frankreich,
Ilalien,
Inaugural-Dissertation,
Universitiit Munster.
Schat,
H.
involved
der
strain
type
stress.
Cadmium-binding peptides
Ackerley,
in
mature root cells.
Sasse,
Ann. Bot. 61: 723-726.
(1934):
Kupfer.
a
(1986b):
104: 671-679.
&
meristem
on
zinc-tolerant and
rubra L.
M S.
wild
a
copper
metallpflanzen. Inaugural-Dissertation Universitat
D.
non-tolerant
Phylol.
H.D.
character-
the root
nuclear and nucleolar
and
Kumar,
in
content in the root meristem of
Festuca rubra L. New
&
Unlersuchungen
Phylol.
Francis,
and
under
Rauser, W.E. & Curvetto, N.R.
gische
M.J.,
J.B.
(1986a):
419^28.
Powell,
Cell
D.
non-tolerant
a
New
Plant
biochemical
and
(1991):
W.E. &
Riither.
Francis,
&
tissue
Methods in enzymology 205: 319-333.
of cadmium
Robinson,
A. &
L. Plant Sci. 42: 61-66.
M.J.,
meristem
plants.
nein-like
accumu-
odoratum.
in
138:68-74.
W.E.
Robinson,
role of the cell wall in the mechanism
(1985): The
cultivar
zinc-65 in
22: 653-661.
Sci. Total Environ.
Powell,
of
Fontinalis
by
doliolum
lation and
A. stolonifera L.
Poulter, A., Collin, H. A., Thurman, D
of
bertolonii
Alyssum
1641-1642.
K.
tolerance
82.
copper tolerant
a
Physiol.
Rauser,
Repp,
Puia,
of
Plant.
Porter, E.K. &
K.
the
20: 863-875.
uptake
Physiol.
lation
compounds
Biol. Chem. 40:
D.C, &
Pickering,
the
Galoppini,C.(1976): On
tenuis Sibth. and
Agrostis
of
Anabaena
Reilly,
R. &
Anthoxanthum
H. SCHAT
Hardwick,
Metal
L.C., Mallick, N., Singh,
Reese,
in
H.A.,
(1981):
(1991): Physiological
Reese,
of
(1979): Sensitivity
(1973): Multiphasic uptake
Mineral
chelating
Oxford.
McNeilly,
Phylol.
Natural
(1973);
polymers. Pergamon Press,
rooting
1:80
occurs
Muzzarelli,
Nicholls,
of
Rauser.
spectra
Collin,
D.A.
Reports
Rai.
C. VERKLEIJ AND
J.A.,
culture
from
of CD-binding peptide I from
pomhe.
43-50.
1985),
Edinburgh.
Murasugi, A., Wada, C.
cation and
Metals
(ed.): Heavy
(Athens
A,
Thurman,
istics
substituted roots of metal tolerant and non-tolerant
ecotypes.
J.
ERNST,
Qureshi.
and metab-
sativa
(Oryza
81: 26-33.
Hardwick,
M.,
Heavy
P.
Maitra,
germinating rice
H. O.
merely
&
in
Kalff,
reflect
(in press).
M.
differential
(1992):
metal
Are
phytochelatins
tolerance,
metal-imposed strain?
or
Plant
do
they
Physiol.
METAL TOLERANCE
Schat,
&
H.
control
H.
tolerance
copper
Heredity 68:
Schat,
&
247
(1992a):
Genetic
Silene
vulgaris.
in
219-229.
Ten
tolerance
Metal-
(1992b):
syndromes
Scheller, H.V., Huang, B., Hatch,
(1987):
Phytochelatin
thione levels in
cells.
Plant
K.B
Searcy,
response to
Physiol.
&
in
higher
Goldbrough,
and
synthesis
heavy
D.C.
metals
gluta-
in tomato
Pollen
for
tube
tolerance
metal
(Caryophyllaceae)
and
Amer.
in
Mimulus
J.
Bot.
72:
1695-1699.
selection
&
and the
tolerance
in
Silene
72: 700
metal
of
sporophytes
Krause
tolerance
Silene
and
The
dioica
parallel
pollen
(L.) Clairv.,
Mimulus guttatus
S.
DC.
B.B.
(1991):
effect
Phytol.
N. &
Stewart,
G.R.
der
Van
Beauv.
cespitosa! (L.)
Van
J.C.
ance
Van
Deschampsia
and Anthoxanthum odoratum.
The
(1990):
heavy metal-binding pepMot. Biol.
Physiol.
Accumulation
of
&
B.G.
Williams,
(1986):
non-protein metal-binding poly-
peptides (y-glutamyl-eysteinyl), glycine
in
selected
cadmium-resistant tomato cells. J. Biot. Chem.
261:
13879-13882.
J. &
Strange,
role
for the cell
M.R.
(1991):
membrane
Mimulus guttatus Fischer
in
Evidence
tolerance
copper
DC. New
ex
for
Phytol.
a
of
119;
383-388.
Thurman,
D.A.
In:
Proc.
&
Int.
in
(1983):
Metal
higher plants—review.
Conf. Heavy
Heidelberg,
ment,
J.C.L.
Collins,
mechanisms
Metals
298-300.
in
CEP
the Environ-
Consultants,
Edinburgh.
PsMt,
in
N.J.
E.
R.G. &
radioisotopes
in
plants.
Physiology.
to
of the pea
&
Van
R.P.G.
(1967);
investigate heavy
Isotopes
I.A.E.A.
(1990):
and
in
Vienna,
Plant
The
(1987):
a
D.
zinc in
metal
493-508.
and
metals
Doctorial
(1976):
Chemical
phloem
exudates.
M.E.
Stevenick,
metal
&
toler-
(Zn, Cd)
(Lemna minor).
Steveninck,
Van
L.B.
Edwards,
Electron
in
a
probe
Zn tolerant
X-ray
clone
R.F.M..
D.R.,
&
M.E,
Wells,
A.J.
microanalytical
of
of Lemna minor
Van
zinc
L.
Ill, 671-678.
W.J.
Horst,
Deposition
Steveninck.
&
M.E.,
W.J,
Marschner,
in
phytate
globular
caespitosa
mechanism? J. Plant
ance
A.J. &
and
Lemna
Van
D.R.
the
minor.
Physiol.
Veltrup,
of
R.F.M.,
Fernando,
Steveninck,
Wells,
W.
ecotypes;
Physiol.
131:
binding
Steveninck,
(1990b):
of zinc
as
zinc
X-ray microanalytical
M.E.,
Zinc toler-
phytate
in
evidence.
J.
137: 140-146.
(1976): Concentration-dependentuptake
by
copper
barley
roots.
36:
Plant.
Physiol.
217-220.
Veltrup,
W.
(1977):
The
uptake
of
Z.
presence ofzinc.
by barley
copper
Pflanzenphysiol.
83:
201-206.
Veltrup,
Nutrition
13:
247-257.
barley
tolerance
R.F.M.,
detoxification
Veltrup,
of
in
Effects of metals
higher plants.
bodies in roots of Deschampsia
gene
use
tolerance
Plant Cel! Environ.
Van
R.F.M.,
Steveninck,
of the
FEBS Letters 292: 48-52.
Gregory,
In:
A., Urwin, P.E.
Metal-binding properties
expressed protein.
Turner,
W.
(1991): Expression
coli.
H.
plants.
Wiersma,
D.R.,
roots in the
Toramey, A.M., Shi, J., Lindsay,
Robinson,
19-33.
Acad. Sci. Paris 310: Ser.
Plant
tolerance
in
of lead
26:
evidence for two distinct mechanisms of Zn and Cd
Van
Macnair,
of
zinc tolerance.
to
(in press).
Fernando,
D.F.
accumu-
of roots
36:213-216.
Steveninck,
C.R.
41: 553-575.
The
fractions
in selected clones of duck weed
binding
tides of plants. Anna. Rev. Plant
Steffens, J.C, Hunt,
&
Steveninck,
Plant Soil
107; 659-670.
Phytol.
Steffens,
of
zinctenuis
Universiteit Amsterdam.
Plant.
(1990a):
New
Clijsters,
activity
manganese
tolerant
clones
of
Agrostis
(1972):
Genetics
Heredity
BJ.
Fernando,
non-tolerant
of
in relation
and terrestrial
Goor,
Physiol.
syn-
accumu-
Werff, M. (1981): Ecotoxicity of heavy
thetase and ammonium assimilation in roots of zincand
C.
subcellular
(1971):
F. &
aquatic
alba
40: 133-138.
The
(1971):
homogenates
195-206.
forms of
Theor.
Glutamine
(1987):
69:
Phylol.
71:671-676.
C.
enzyme
and
sunflower
on
of
70: 539-545.
tenuis Sibth.
Assche,
on
C.
root
Fernando, D.R.(I992): Heavy
Nickel
New
Sibth.
Marshall,
by
Festuca ovina.
in
in
leaf cell membranes. Acta Bot. Neerl.
Smirnoff,
&
of zinc
Urquhardt,
Van
Genetics 69: 597-602.
Slivinskaya,
New
by
Phytol.
R.G.
Agrostis
and
(1985c):
tenuis
non-tolerant clones
Thesis, Vrije
D.C.
distribution
the roots of metal-tolerant
Marshall,
65-Zn
Sibth. New
Turner,
Amer. J. Bot.
(Caryophyllaceae)
(Scrophulariaceae).
Mulcahy,
of
expression
Appl.
of metal
706.
K.B. &
(Mill.)
diocia
Pollen
(1985b):
gametophytic expression
Mimulus guttatus
Searcy,
D.C.
Mulcahy,
of
tolerant and
Van
K.B.
Searcy,
within
Agrostis
R.G. &
Turner,
lation
(1985a):
(Scrophulariaceae).
guttatus
E. &
The subcellular
(1970);
copper
of
lation
1031-1035.
selection
and
dioica
Silene
85:
Mulcahy,
competition
zinc and
725-731.
plants. Serpentine Ecology (in press).
P.B.
R.G.
Turner,
clones
W.M.
Bookum,
of metal
specificity
W.M.
Bookum,
Ten
of
IN PLANTS
on
the
W.
(1978):
roots.
W.
(1979);
uptake
of
Pflanzenphysiol.
Verkleij,
and
Plant. 42:
copper
by
of zinc
uptake by
190-194.
The effect ofNi
93: 1
J.A.C. &
tolerance
Characteristics
Physiol.
2+
intact
2+
,Cd
,
barley
and Co
roots.
2+
Z.
9,
Bast-Cramer,
multiple heavy
W.B.
metal
(1985):
Co-
tolerance
in
248
W.
Silene
cucubalus
T.D.
Lekkas,
Athens
ment,,
from
different
174-176.
1985,
metal
heavy
Metals
(ed.) Heavy
the
in
CEP
H.
O.
sites.
Environ-
Consultants,
Edinburgh.
Genetic
cucubalus
luted
D.
107-114.
In:
in
studies
occurring
areas.
Rudin,
on
Scholz,
of
Koevoets,
Air
Effects of
unpol-
H.R.
and
J.A.
&
de
Brumold, C.,
Nutrition
In:
L.J.
Kok,
The
of
role
and
J.
Stulen,
Academic
in
Bladder
Rennenberg,
Assimilation
Sulfur
SPB
in
H.,
(eds):
Higher
The
Publishing,
Rossenberg,
M.C.,
tolerance
D.
Winge,
van’t
P.,
R.
Bank,
Verkleij,
ance
mechanisms
and
Hamer.
Molecular
Homeostasis:
347-357,
Alan
R. Liss
J.A.C. &
&
Riet, J.,
W
Ernst,
(
=
of Silene
D.
van
H O.
Meta!
and
Biology
J.E.
(1989): Cadmium
in
S. cucubalus
Silene
Ion
Chemistry,
New York.
Prast,
the
cucubalus.
(eds):
Inc.,
and co-tolerance
Garcke
toler-
vulgaris (Moench)
(L.) Wib.).
New
Phylol.
Ill:
Metal
Heavy
Aspects,
localization
&
of
in
Wagner,
GJ.
leaves.
Mechanisms
In; Shaw, A. J.
Plants:
Press,
Wagner,
tobacco
92:
in
Boca
G.J,
cadmium
function for
Physiol.
(1990):
higherplants.
Tolerance
179-194. CRC
Vogeli-Lange, R.
peptides
H.
Schat,
metal tolerance in
port
(ed.):
Evolutionary
Raton,
FI.
cadmium-binding
Implications
of
a
trans-
Plant
cadmium-bindingpeptides.
of
cabbage
of
leaves.
a
cadmium-
Plant
Physio).
76: 797-805.
Wainwright,
S.J. &
Woolhouse,
M.J.
Chadwick,
and
Resource
Ecology
of
231-259.
Blackwell
Wainwright,
of
S.J. &
in
Agrostis
Watkins,
tenuis
A.D. &
66: 47-54.
tolerance.
G.T.
of
H.W,
and
cell
exp. Bol.
M.R.
The
Oxford.
(1977):
Some
zinc tolerance
elongation
28:
In:
Renewal,
Publications,
copper
Sibth.;
(eds):
and
Degradation
Macnair,
in
(1975): Physio-
metal
Woolhouse,
damage. J.
arsenic tolerance
H.W.
Goodman,
Scientific
physiological aspects
membrane
heavy
and
1029-1036.
(1991):
Agrostis capillaris
Genetics of
L.
Heredity
distri-
in
bean
65: 480-482.
A.M, &
in
R.L.
Chaney,
(1981a):
Chemical
I.
fluid.
xylem
tomato and
Plant
stem exudate.
soybean
R.L. &
67:
Physiol.
of
lead
3.
(1981b):
Electrophoretic
311-315.
A
(1957):
A.M.
Decker,
for
technique
tolerance
in
plants.
the
Nature
180, 37.
Wilkins, D.A.
to
edaphic
(1978):
factors
J.B.
Wilson,
tolerance:
H.W. &
of
In:
R.D.
H.W.
Responses
copper
physio-
tolerance
and
A.D.
Plants,
Sydney.
to
Osmond,
Plant
the
to
The
(1981);
and
and
Toxicity
plants
(eds): Encyclopedia of
C.
S.
Loneragan, J.F., Robson,
of
P.S.,
Nobel,
heavy-metal
(eds): Copperin Soils
(1983):
responses
of
cost
toxicity
Academic Press,
Woolhouse,
the
New
growth.
Evolution 42: 408-413.
Walker,
copper
higherplants.
235-262.
The
example.
and Graham,
in
of root
means
(1988):
an
logical basis
in
The measurement of tolerance
by
80: 623-633.
Phylol.
tolerances
In:
metals.
C.B.
and
N.S.
Physiology
Chemical
Lange,
Ziegler,
and
H.
XII,
Biological
Environment, 245-300. Springer Verlag, Berlin.
L.
in
contaminated
Metal
Heavy
Aspects.
L.
Colonization
(1990):
plants
&
Wu,
L.
&
in
Tolerance
establishment
In:
A.J.
Shaw,
Plants:
Evolutionary
Antonovics,
(1976): Experimental
in
Plantago.
lanceolata
Ecology
J.
and
of
(ed.):
Press, Boca
Plantago
roadside.
and
sites.
259-284. CRC
logical genetics
Raton,
FI.
eco-
tolerance
II. Lead
in
from
Cynodon dactylon
a
57: 205-208.
Antonovics,
J.
(1978):
Zinc
L.
Agrostis stolonifera
and
copper
in tissue culture.
Amer. J. Bol. 65; 268-271.
D.A,
Wu, L., Thurman,
The
mechanisms
cadmium
67: 292-300.
D.A.
tolerance of
(1984): Characterization
of
complexationin xylem fluid.
measurement
Wu,
Subcellular
(1990):
and
of
1086-1093.
binding complex
logical
Physiol.
Subcellular
(1980):
form
Physiol.
White, M.C., Chaney,
Wu,
J.A.C. &
HJ.
Jager,
chemical
composition of
Plant
O.L.,
637-645.
Verkleij,
VERKLEIJ AND H. SCHAT
complexation
Woolhouse,
J.A.C., Koevoets,
(1989b): The roleofmetal-bindingcompoundsin
In:
Metal
Wilkins,
Hague.
copper
Plant
de
Riet, J.,
(1990):
mechanism
vulgaris).
and
255-260.
Verkleij,
plants.
evidence.
van’t
W.H.O.
Ernst,
Campion (Silene
Plants,
&
and
Metal
Springer Verlag Berlin.
cadmium-tolerance
Sulfur
H.J.
bution
Pollutants,
metal-binding compounds (phytochelatins)
the
P.
of Silene
and
polluted
F., Gregorius,
Genetic
(eds):
&
populations
various
Verkleij, J.A.C., Koevoets, P.L.M.,
Knecht,
Weigel,
A. C.
White, M.C., Decker,
W.B.
Verkleij, J.A.C, Bast-Cramer,
(1989a):
J.
ERNST,
uptake
&
Bradshaw,
and
processes
of
clones
Agrostis stolonifera.
of
A.D.
(1975):
of copper and its affect upon respiratory
copper-tolerant
non-tolerant
New
Phylol.,
75:
225-229.
Wyn Jones, R.G., Sutcliffe,
Physiological
metal
tolerance
Samish,
Nutrition
Publ.,
and
R.M.
2:
New
in
clones
(ed.);
575-581.
York.
M. &
Marshall, C. (1971):
biochemical
of
Recent
Gordon
basis
for
Agrostis
Advances
&
heavy
tenuis.
Breach
in
In:
Plant
Science