Response of higher plants to lead contaminated environment

Chemosphere, Vol. 34, No. 1l, pp. 2467-2493, 1997

Pergamon

© 1997 Elsevier Science Ltd

All rights reserved. Printed in Great Britain 0045-6535197 $17.00+0.00

PII: S0045-6535(97)00087-8

RESPONSE OF HIGHER PLANTS TO LEAD CONTAMINATED ENVIRONMENT Rana P. Singhl, Rudra D. Tripathi 2., S.K. Sinha3, Renu Maheshwaril and H.S. Srivastava4 1 Department of Biosciences, M.D. University, Rohtak-124 001, India. 2 Environmental Botany Laboratory, Environmental Science Division, National Botanical Research Institute, Lucknow-226 001, India 3 Biotechnology Division,UP.C.ST., B-144,Sector C, Mahanagar, Lucknow-226006 4 Department of Plant Sciences, Rohilkhand University, Bareilly-243 006, India. (Receive.d ila Japan 17 February 1996; accepted 14 January 1997)

ABSTRACT

Lead

concentration

is

increasing

rapidly

in

the

increased use of its sources by human society.

environment

due

to

Alarming concentrations of

the metal have been reported in dust of densely populated urban areas and, water Plants

and

land

absorb

roots, stems, increase

of

various

lead

and

accumulation

the

exogenous

productivity

and

the

plant

near

the

of

industrial

the

metal

waste

have

been

disposals. reported

in

leaves, root nodules and seeds etc. which increases with the

in

species.

areas

and

level.

magnitude

Photosynthesis

processes

lead

has

the

of

been

the

found

effect

Lead

of

affects

effects to

the

be

depend

one

metal

plant

of

is

the

growth

upon

the

most

and plant

sensitive

multifacial.

Nitrate

reduction is inhibited drastically in roots by the metal but in the leaves a differential effect is observed in various cultivars. Lead also inhibits nodulation,

N-fixation

and ammonium

appears that the toxic level

and

provision

assimilation

effect of the metal

of

certain

inorganic

in the root

nodules.

It

is primarily at physiological

salts

can

antagonize

the

toxic

effects to some extent. Further responses of plants to the metal depend on various endogenous, able

to

tolerate

environmental and nutritional factors.

excess

compartmentalization

of

or

Pb +2

by

synthesizing

involving

processes

metal

detoxifying

Some plants are like

exclusion,

peptides-

phytochelatins. © 1997 E l s e v i e r S c i e n c e Ltd

•Author for correspondence.

(Fax: 0522- 282881, 282849). ( Email: manager@ nbri.sirnetd.ernet.in) 2467

the

2468 INTRODUCTION

The

systematic

other

biological

effects

of

animal

the

in

for their

other

have

higher

plants

to

the

another

direction

metal

(Thapa

et al., up

the

where

of

The

SODRCES

al.,

the

1988,

of

derivatives

in

exhaust

the

extensive flora

lead

LEVEL

Certain

plants

including 1989).

of

the

of

years.

a

as to the

their

of important

thorough

analysis.

amendments

physiological

of

genetic

and

may

be

with the

biochemical

forest trees have been reviewed

However,

to

detail

(Broyer et

and responses to

various

several

understand

new

the

studies

responses

plant species,

1976).

which

are

lead of

include

Another

cracked

aerosols

the

roadside

metal

and phosphate

metal

have

of

the

to the metal.

is

often

major

to

near

side.

in

lead

is

lead

1971).

Pb +2

based

(Lagerwerff

source

release

road

rich

smelting,

fertilizers

(Smith,

1970; Motto et at., 1970;

environment

industrialization

Recently

El Hussanin

Pb +2

Egypt

shown

had

is

been

soils

lead

in

The

results

soil

content

et

alkyl

automobile

This

Page & Ganje,

static

total

and

urbanization

(1993)

have

in

and

the

(Cannon

and

1970).

with

tended

has

been

during

shown

in Abu Rawash

irrigated

that the metal

at 0-10 cm depth,

not

and

et al.

in the sandy

which

They have

layer where

al.,

of

i'n the

to

and available areas

some

and potential needs

to

plants.

IN T H E E N V I R O N M E N T

lead due

decades.

et

form

1962; Chow,

rapidly

in

the dicots

according

with

in several

pesticides

contamination

OF LEAD

Level

of

are to be find out to counter

contamination

gasoline

inhabiting

Bowles,

studied

toxic

related

those

to the metal

vary

toxicity

possibilities

Goldsmith

in

than

and

the

studies

to be toxic to the plants

plants.

Pahlsson,

better

plants

although

than

metal ~ toxicity

principles

lead arsenate,

1973;

been

on

OF LEAD

sources

paints,

have

in general

however,

the

Pb +2

The

extensive

of the plants

may,

plants and mechanism of tolerance MAJOR

time.

make up. The trend of effects

to

the

monocots

sensitivity

of lead on higher

opened

more

of

sixties

long

is considered

reversibility

toxicity

effects

the

effects

late

for

to heavy metals

tolerate

Further

in

known however,

processes

and physiological crop

been,

lead

forms, plant

started

were

plants

Though

life

different

physiological

systems

responses

1972).

on

metal

systems

Further,

al.,

studies

an increased

sewage

water

Further Akhter

and Madany

(1993)

697.2 mgg -I Pb in street dust and 360.0 mgg -I metal

dust

of

Bahrain

which

was

highest

amongst

Pb,

Zn,

Ni

total

EI-Asfar

for

upto

67

from 11.4

during

have estimated

i.e.

few

in the surface

Pb +2 increased

mgL -I to 49.2 mgL -1 and 0.7 mgL -I to 3.0 mgL -1 respectively of irrigation.

last

and EI-Gabal

to accumulate

and available

increasing

the

5 years

a very high

in the house hold and

Cr,

the

toxic

2469 metals

detected.

various

He has

countries

Jamaica,

Kenya,

and

Kuwait,

the environmental Bahrain, New

dust

Canada,

Zealand

have

(Forstner

Wittman,

varied

from

UK,

the

water

Scotland

that

countries

and Taiwan

have

in dust

like

USA,

West

Germany,

level

upto

17.9

Malaysia,

mgg -I

dust

of

Greece,

lesser Pb +2

from 4.1-9.50 mgg -I dust whereas

generally

1979)

global

0.001

levels of the metals

appeared

areas

Netherland

in certain

in of and

areas

1993).

fresh

and

Nigeria,

a maximum

Uncontaminated that

summarized

clearly

ranging

Egypt,

(Akhter and Madany,

revealed

also it

to

and

range

0.06

a of

mgL -I.

has

a

lead

study

content

conducted

Pb +2

by

working

pond system having nonpoint source pollution,

out

0.003

mgL -I

UNEP/WHO

concentration

While

of in

(1977)

ground

metal

water

pollution

of

the Pb +2 level was found to

be as high as 1.4 mgL -I and this water was used by cattles and for bathing purposes

(Chandra et al.,

by rural people

scientists

of

CCS

Agricultural

1993).

University,

In an estimation

Hissar,

India,

the

by the

level

of

Pb +2 in Haryana soils was found to range from i0 to 22.5 mg kg -I in canal irrigated water

soils

and

7.5-22.5

(Kuhad and Malik,

Haryana

soils

had

mg kg -I

1989).

a lead

in the

It was also

level

of

i0 to

soils

irrigated

with

found that different

10.5 mg

kg -I

sewage

types of

(Kuhad and Malik,

1989). In a study, when

6.44

Bg g-i

pb+2

was

detected

it was grown on sewage sludge while

in shoots

Panicum

of

maximum

0.85 ~g g-i pb+2 was found when

it was grown at an uncontaminated site. Various water bodies have also been reported to be contaminated with high level

of

lead.

Lead concentration

(Hyderabad)

has

that

water

ground

been

reported

collected

in water

to

from

be

0.038-0.062

radius

0.028 mgL -I which was reduced upto

samples of Hussain

of

use

is centaminated of

Pb +2

Haryana,

containing

Punjab

contamination accumulation

from

and

upto

the

industrial

pesticides

West

U.P.

hazardous

and

it was

m was

having

0.001-0.009 mgL -I water

wastes

during

in

level

green

India which

of

has is

the

1973). The

city.

Increasing

revolution caused

evident

package

soil

and

a

higher

by

found 0.007-

in the ground

(Srikanth et al.,

water from radius of 1000-2000 m of the lake lake

mgL -I

200-1000

Sagar Lake

in

water Pb +2

in the plantation without any exogenous Pb +2 supply in these

areas (Kumar et al., 1994; Dabas, 1992; Bharti and Singh, 1993). The

metal

coating 1976).

on

remains plant

largely surfaces

Mostly

lead

contain

5-200

times

(Smith,

1971).

as

a

associated higher

Pubescent

superficial

(Schuk lead

and

with for

Locke,

deposit 1970;

foliage

as

unwashed

leaf

a

or

topical

Zimdahl topical surfaces

leaves have been coated with more

and

aerosol Faster,

coating of

the

may crop

lead than the

2470 smooth

surfaced

leaves

possibly

due to regular wash off

of the metal

by

the rain water from the smooth leaf surface (Zimdahl and Koeppe, 1977). UPTAKE OF LEAD BY P L A N T S

Lead in the soil is present in the form of soluble and insoluble salts and is tightly either

bound

to

the

air

from

colloidal or

mostly as a component

organic

from

the

of the dust

molecules.

Plants

aerosol

The

fumes,

and moist vapour,

the

The

lead

plants

growing

because

of

the

on the

road

release

of

side

lead

are

from

(Wallace et al., Plant roots

1974; Goldsmith et al.,

which

get deposited enriched

autovehicles

and

level

1976; Wheeller and Rolfe,

are able to extract some of this metal

conditions

1972;

such

et

Miller

as

al.,

1975a,b;

Laerhoven,

1976)

and

al.,

1976;

Sung,

1976;

soil

solution.

with tissue and P.

other

uronic

of

acid

exchange

Pb

Faster,

and

Reinbold,

al.,

1994a)

in cell

al.,

(Baumhardt

and

content

(Kought et

capacity

(Rolfe

et

wall

in aquatic 1961;

alter

and

1976;

1976). Various

and

Welch,

John

1977;

lead

free

plant,

Welsh,

of

from soil and culture

Zimdahl

ions

Singh

Loading

crispus

cation

with

from the highway border

solutions but translocation to aerial part is generally limited. soil

lead

exists

(Zimdahl and Koeppe,

especially

Pb +2 in plants decreases with increasing distance

absorb

lead,

on the leaves and other exposed surfaces of the plant 1977).

may

soil.

and

Van

Karmanos

uptake

from

et the

space was

correlated

Pctamogeton

pectinatus

1977).

In ageing macrophyte

tissue, there is evidence of increasing surface area and number of exposed lead binding Denny, to

sites which

anionic

associated

space

(Sharpe and Denny,

reduced

sesame

Cd +2

roots

amount

orthophosphate and

of

1966;

triamine

it

versa

interfered

with

agents

such and

pentaacetic

as

EDTA

acid

Toxicity and

of

cellular

enriched

lead

to

large

localization.

environment

extent

and

increases

are able to accommodate

and

Na +

Existance of

the

lead

but

uptake

et

in

uptake

al.,

the

(Martin 1976).

uptake

and

1977).

PARTS

upon

plant

lead

Wallace

the

In maize,

1977)

absorption,

increases

also

depends

wall-

1991).

al.,

Cu +2

lead

1971;

IN P L A N T

Susceptible

cell

precipitates

translocation of lead in barley plants (Patel et al.,

ACCUMEW-2&TION A N D IX)C.ALIZATION O F L E A D

(Sharpe and

unpublished results).

reduce

Crowdu,

et

Cd +2,

insoluble

pyrophosphate

with

Guilizzoni, (Miller

S.K.,

phosphate,

Tanton

substances

1976;

vice

for Pb

Lead presumably becomes complexed

pectic

and Sinha,

of

lead

chelating

Hammond,

Diethylene

and

N.

with

and

leaves,

Bharti,

abundant

presence

uptake

and

(Singh, R.P., of

1978).

sites

Donnan-free Pb +2

increase the uptake capacity

1970; Odum and Drifmeyer,

its

absorption,

species

growing

large q~antities

transport in

a

lead

of lead

in

2471 their

organs

et al.,

(Johnson

19771

Johnson

and Procter,

19771

Kumar

et

al., 1993 ; Bharti and Singh, 1993). Plants of Cassia tora and C. occidentalis growing by the road side accumulate upto 300 mg g-i dry wt. of

lead

(Krishnayapa

upon the species,

and Bedi,

1986).

plant cultivar,

The

accumulation

of

lead depends

plant organ, the exogenous concentration

of lead and the presence of other ions in the environment. Accumulation in roots and leaves of cv. HT-I, a sensitive variety of Sesamum indicum L. is about 20 times higher than those

al.,

1993 ;

Bharti

and

Singh,

(Kumar et

in the resistant variety PB-I 1993).

Symbiotic

root

nodules

Vigna

of

radiata L. cv. Pusa baishakhi accumulated significantly high lead level in the

growing

plants

exogenously the

added

increased

raised

lead

with

and

exogenous

unpublished results).

the

lead

Hoaglands level

level

of

nutrient

(Dabas,

In most cases,

solution

endogenous S.,

metal

Singh,

without

increased

R.P.

and

an

with

Sawhney,

it has been reported that the roots

accumulate higher amount of the metal than the shoot and leaves (Table I).

Further, the accumulated lead content generally increase with the increase in the metal leaves

in the

(Sinha,

environment

inorganic salts such as

1993;

toxicity. effect.

K2HP04,

localization

Accumulation In

onion

orthophosphate

pectinatus,

the

(Dabas,

metal

is

an

is

(Tandler

gets

1992)

and

1993).

and pea

sesame

roots

The presence

of and

(Singh et al., 1994a).

Pb +2

(Sharp and Denny,

for maize

CaCI 2 and KNO 3 restrict Pb +2 uptake

metal

nucleolus

the

equilibrium

of

reported

important

inside the vacuoles may

tips,

in

been

Bharti and Singh,

accumulation by mung bean seedlings

Intracellular

has

Vigna root nodules

1990),

(Kumar et al.,

and leaves

as

bound 1976).

not cause

reported and

to

to

Solari, cell

determination be

its

any deleterious

localized

as

lead

In Potamogeton

1969).

wall,

in

probably

by

Donnan

At 0.5 ~M Pb +2 Vallisneria spiralis

accumulated 1.41 ~mole pb+2g -I and at 1.00 ~M Pb +2 the accumulation was 2.5 times

higher

than

at

0.5

~M

Pb +2.

The

Pb +2

concentration was more in roots than in leaves At

I00

high

as

~M

Pb +2

5.04

level, ~mole

the

g-i

lead

dry

content

wt

level

back

ground

(Gupta and Chandra,

at

1994).

of Hydrilla

(Gupta

and

each

verticillata was

Chandra,

1994).

Lead

also

disturbs the chromosomal region which vary with the lead concentration,

Lactuca

sativa

(Sekera

and

Bapak,

1974).

The

metal

caused

as in

spindle

disturbances in root tip cells of Allium cepa (Ahlberg et al., 1972).

SEED GERMINATION

Seed germination life

of

a

AND

SEEDLING

GRONTH

and early seedling growth are the

plant

projecting

the

extent

of

initial events

future

in the

physiological

and

2472 biochemical

processes.

Seed

germination

is

initiated

with

regulation

of

enzymatic reaction which activates catabolic and anabolic processes in the storage

tissues

Germination affected.

The

inhibited

Lead

germination

sativa

(cotyledons

is

and

if

and

in

one

component

in

the

soil

contamination

in Spartiana

endosperm)

even

alterniflora

the

of

is

known

inhibition of germination

by exogenously

axis.

processes

to

inhibit

is seed

1982), Oryza

(Morzek and Funicelli,

1976) and Vigna radiata

(Mukherjee and Maitra,

embryonic

these

(Dabas, 1992).

supplied

Pb +2 is a possible

effect of interference with some important enzymes involved in the process (Mukherji and Maitra, Mitra

(1976)

activities supply.

have

1976; Van Assche and Clijsters,

reported

by

about

There

is

50% 34%

an

in

inhibition

rice

decrease

of

endosperm in

fresh

the

due

to

weight,

1990). Mukherji and

protease higher a

23%

and

amylase

level

of

decrease

Pb +2

in

dry

weight and 26% decrease in chlorophyll content in oats when seedlings were grown

for

21

days

in

a

(Fiussello and Molinari,

Low

concentration

of

nutrient

solution

containing

10 -4

M

Pb

(NO3) 2

1973).

lead

(5 pM)

caused

a very

significant

reduction

in

the development of stele in explants of lettuce and of secondary phloem in carrot

roots

(Barker,

caused

death

of

1972;

Bradshaw

inhibitory

the

1972). plants

and

effect

of

coleoptile

elongation and

of

Vigna

1993).

the

The

effect

cell

embryonic

axis

(Dabas, of

lead

1992; on

Symeonidis

may

also

growth

and

(Bradshaw,

et

arise

al.,

from

ultimately

1952;

Barker,

1985).

The

interference

elongation which has been demonstrated

et

(Lane

root

species

1981;

lead on growth

assay

radiata

inhibited

several

McNeilly,

Pb +2 with auxin regulated

Arena

Lead in

al.,

1978).

has

drastic

also

been

shown

et

al.,

1993;

Kumar

fresh

A

and

dry

biomass

decrease

in

in Sesamum Bharti

of in the

indicum

and

Singh,

accumulation

of

the

plant parts seems to be differential with regards to plant species,

plant

(Kumar et al.,

1993;

cultivars, Bharti plant

plant organs

and Singh, cultivars

1993,

showing

and the metabolic 1994; the

Singh

processes

et al.,

tolerance

to

1994a,

Pb +2

may

other toxic metals like Cu +2 and Cd +2 and vice versa Bharti

and Singh,

is not

shared

for

1994) the

and

be

very

Further, sensitive

(Singh et al.,

the to

1994b,

it appears that the same tolerance mechanism

related

toxic

seems to be

in fresh wt.,

reversible

dry wt.

well as

as

plants

for

in Vigna

the

may

possess

Effect of Pb +2 on biomass accumulation of root and aerial parts seedlings

as

thus

metals.

reduction

lead

and

response

337,

for

metals

specific

of growing

mechanism

1994b).

other

radiata

toxic

var.

ML-

and length of root and shoots could

be recovered almost completely by the addition of i0 mM K2HPO 4 and to some extent by CaCl 2 in the nutrient medium (Singh et al., 1994a).

2473 Table

i.

Accumulation

Plant Species

Plant parts

Lead supplied (mM)

Roots Pisum sativum L. cv. Aranchal

0.0 0.5 0.0 0.5 0.0 0.5

5

0.0 1.0 0.0 1.0 0.0 1.0

5

Root Nodules

0.0 1.0

34

Roots

0.0 1.0 0.0 1.0

5

0.0 1.0 0.0 1.0 0.0 1.0

14

Roots Shoots Leaves

Roots Shoots Leaves

Vigna radiata L. cv. Pusa Baisakhi

cv ML-337

Leaves

Roots Zea mays L. Shoots cv. Ganga Safed 2 Leaves

PHOTOSYNTHETIC

Photosynthesis processes different American

al.,

14

is

5

1.95±0.05 253.0 ±2.0 0.08±0.01 131.0 ±i.00 1.30±0.10 86.20±0.20

5 5

1990

Sinha,

1990

Kumar et al.

1993

Kumar et al.

1993

Kumar et al.

1993

1995

Singh et al. 1994a Singh et al. 1994a

67.5±0.08 365.0±0.8 32.0±0.4 250.5±0.1 33.5±1.07 72.5±0.8

14

Sinha,

Dabas et al.

114.0 1970.5 128.0 460.5

14

1990

Bharti and Singh, 1993 Bharti and Singh, 1993 Bharti and Singh, 1993

2.05±1.0 64.10±0.05

5

considered

plants,

1972).

24.0±2 6577.0±75 1.3±0.5 723.3±7.5 17.0±10 1452.7±18.5

Sinha,

Sinha,

1990

S¥STEK

sycamore to

43.5±0.0 192.5±0.0 26.0±0.1 132~5±0.001 27.0±0.002 372.0±0.4

5

species.

Lead content References of the plant (~g g-i dry wt)

14

of Pb +2 toxicity.

photosynthesis reported

Age of the plant (days)

14

Leaves

cv.PB-I

in p l a n t p a r t s of v a r i o u s

0.0 1.0 0.0 1.0 0.0 1.0

Shoots

Sesamum indicum cv. HT-I

of Pb +2

for

example,

(Carlson et al.,

was

inhibit

inhibited

by

photosynthesis

Reduction

following reasons:

as

in

one

The metal

leaf

in

of

the

most

inhibits

soybean

sensitive

rate

metabolic

of photosynthesis

(Bazzaz

et

al.,

1975)

in and

1977).

At 193 ~M leaf Pb +2, the rate of

about

50%.

in the

The

isolated

photosynthesis

by

metal

has

chloroplasts lead

may

also

been

(Miles be

due

et to

2474 Table

2.

Plant species

Nitrate reductase

Plant parts

activity

Pb +2 Age of supplied the plant (mM) (days)

in plant parts during Pb +2 supply.

NRA ~mole NO2-1h-lg-i F. wt. in vivo In vitro

References

Pisum Leaves sativum L. cv. Aranchal

0.0 1.0

14

1.80±2.0 0.65±0.07

0.165±0.01 0.133±0.02

Singh,

Sesamum indicum cv. HT-I

0.0 0.5 0.0 0.5

5

2.4 ±0.II 0.7 ±0.06 2.66±0.1 1.66±0.17

4.1 ±0.3 1.0 ±0.3 5.28±0.13 2.64±0.08

Kumar et al., 1993 Kumar et al., 1993

0.0 1.0 0.0 1.0

5

0.24±0.02 0.12±0.01 0.29±0.02 0.22±0.01

0.78±0.06 1.0 ±0.02 0.73±0.06 1.0 ±0.01

Bharti and Singh, 1993 Bharti and Singh, 1993

0.0 1.0 0.0 1.0 0.0 1.0

34

0.0 1.0 0.0 1.0

5

0.0 1.0

14

Roots Leaves

Roots cv. PB-I Leaves

Vigna radiata L. cv. Pusa Baisakhi

Roots Nodules Roots Leaves

Roots cv. ML.337

Leaves

Zea mays L. cv. GS 2

Leaves

5

5

5 5

5

ND ND 0.845±0.018 0.375±0.095 0.375±0.095 0.ii ±0.05

ND ND ND ND ND ND

1.53 ±0.15 0.72±0.06 0.63±0.07 0.99±0.05

ND ND ND ND

1.31±0.17 1.05±0.12

1988b

Dabas,

1992

Dabas,

1992

Dabas,

1992

(Singh, R.P., Maheshwari, R., & Dabas, S., unpublished data)

2.75±0.58 0.99±0.20

Sinha,

1988a

ND= Not determined i) Closing ii)

of the

Disruption

1974;

Singh,

(iii)

Change

Bazzaz

and

(iv)

stomata

of

the

R.P., in

Kumar,

the of

chloroplast

(Singh,

Inhibiting

i.e., and

chlorophyll

1974;

R.P., and

de

in

total

N.

Chaudhary,

cucumber

and Malik,

N.

photosynthesis

and

1975).

Hanzely,

unpublished

(Hamppe

et

data),

al.,

1973;

Jana,

1987;

Jana

et

al.,

1987).

ions

like

Mg +2,

Mn +2,

etc.

by

Pb +2

in the

G.,

Bharti,

synthesis

the

chlorophyll

(Fiussello

and Bazzaz,

(Rebechiny

and

novo of

Rolfe

Sarkar

Kumar,

plants as in oats 1984),

of

1974b;

organization

carotenoids'as

in vitro degradation

Inhibition

et al.,

Bharti,

essential

data).

(v)

G.,

metabolites

Govindjee,

Replacement

(Bazzaz

chloroplastic

well

pigment level

by

and Molinari, (Burzynski,

N. and Malik,

of

the

as

acceleration

molecules lead

has

1973),

1985),

N.,

unpublished

photosynthetic

(Kumar been

in vivo

et al.,

observed

a q u a t i c plants

dodder

pigments,

during

(Jana

et

1993). in

some

(Jana and al.

1987),

2475 mung bean

al.,

(Prasad and Prasad,

an appreciable have

been

1992;

recovery

Burzynski

and

Prasad

an important

aminolevulinic

acid

porphobilinogen dehydratase

by

and

reducing

(ALAD),

from

delta

tissue

in mungbean

is is

observed

often also

that

depending

carboxylase

taken

inhibited

shown

biosynthesis,

which

catalyses

aminolevulinic In

leaves

that

that the

acid.

the

(Rebechiny

as

a

by

lead

lead

is delta

pathway

of

According

to

lead chloride phosphate

carbon-assimilation

of

1974).

in

Hill

light

reaction

of

pinata

(Sarkar

and

1987). Bazzaz and Govindjee

stimulated

medium.

kinase,

hydrophyte

and Hanzely,

Azolla

in

either

rootless

acid

causes the reduction

measure

(Jana et al.,

upon pH of reaction

and Ribulose-5

photosynthetic

have

of lead nitrate

1987) and Cuscuta reflexa

(1974)

(1987)

hydration.

treatment

in the chloroplast

which

activity

Prasad

enzyme of chlorophyll

demersum

photosynthesis Jana,

of chlorophylls

lead inhibited the activity of delta aminolevulinic

and stroma

activity

level

dehydratase

synthesis

(1985)

Ceratophyllum grana

in the

by the amendment of inorganic potassium salts (Dabas, al., 1994a) and by Mn +2 and Ca +2 (Sinha et al., 1993).

et

(1985)

Burzynski

1993). As reported for the seedling growth,

noticed

Singh

inhibited

1992), maize and pea (Sinha et

1987; Dabas,

b; Sinha et al.,

1988a,

or

Ribulose

inhibited

the two enzymes

are inhibited by

PS

II

1,5-bisphosphate involved

5 mM Pb +2

in

in spinach

extract (Hamppe et al., 1973). NITROGEN ASSIMILATION

Inspite

of being an

studies

have

Nitrate

reductase

assimilation (Venkatraman lead

is

nitrate

Zostera (Sinha

reductase

marina al.,

(Singh,

the

rate

by

1978).

nitrate

also

1993,

R.P.,

and and

sesame

mM

nitrate

in

&

leaves

few 2).

nitrate

Sorghum

reductase The

et

(Huang

1985),

and

very

(Table

overall

in

1984).

soybean

Capone,

R.

in

Pb +2

Grabowaski,

roots

assimilation

lower concentration

1994; Singh et al.,

Maheshwari,

in the plants,

enzyme

i00

and in vivo

inhibited

(Brakup

1988a,b),

to

Relatively

uptake

is

process

to nitrogen limiting

i0

(Burzynski

roots

Bharti and Singh, leaves

(MR),

seedlings

et

with respect

inhibited

et al.,

inhibited

cucumber

important metabolic

been made

maize

activity

in

activity

of

al.,

1974),

pea

leaves

and

(Kumar

leaves

(I00 #/4) of

et

al.,

1993;

1994b) and mungbean roots and

Dabas,

S.,

unpublished

results).

supply of 25 mgL -I Pb +2 increased MR activity in root of Triticum aestivum while 150 mgL -I decreased

it (Bhandal and Kaur,

1992).

It has also been

reported that root and leaf MR activity in some cultivars of Vigna radiata are

regulated

inhibited

differently

significantly

during

the

whereas the

metal

supply

leaf enzyme

i.e.,

root

enzyme

is

is increased wiEh higher

Pb +2 supply (Singh, R.P., Maheshwari, R. and Dabas, S., unpublished data). In

Hydrilla

verticillata

and

Vallisneria

spiralis,

there

was

no

significant effect of Pb +2 on in vivo NR activity at all the concentration

2476 after

24

h

exposure

duration.

However,

increase

in

treatment

duration

resulted in enhanced toxicity on enzyme activity at various concentration and ca. 68% inhibition in V. spiralis and 60% in H. verticillata was found at i00 ~M after 168 h treatment (Gupta and Chandra,

1994).

The inhibition of root NR activity by Pb +2 supply is similar in light and dark,

but the addition

enzyme

activity

R.P.,

in

Maheshwari,

increase

in

light than

of KNO 3 (i0.0 mM)

light R.,

leaf

NR

but

and

not Dabas,

activity

the dark.

in

due

It is also

is able

dark S.,

in

to recover

mungbean

unpublished

to metal

supply

demonstrated

loss

the

in

(Singh,

results).

is more

that

the

seedlings

Further,

pronounced

inhibition

in

in the

root enzyme due to Pb +2 is primarily an interference of the metal

to the

de

can

novo

synthesis

modulated

to

presence

of

unpublished

some

of

nitrate

extent

light

and

results).

by

NO 3

reductase

enzyme

a cytokinin, (Singh,

It has been

and

this

effect

benzylaminopurine

R.P.,

Maheshwari,

R.

suggested that metal

(BAP)

and

be

in the

Dabas,

increases

S.,

leaf NR

activity in Vigna by some allosteric modulation of the enzyme molecule or by

interfering

enzyme,

in

with

vivo

the

activity

(Maheshwari,

of

1993).

some

The

potential

presence

reported from bean leaves (Puranik and Srivastava, Further

cytokinin

(BAP)

activity of mungbean,

induced

recovery

of

inhibitor

of

inhibitor

of has

the been

1985). Pb +2

inhibited

is restricted by chloramphenicol,

root

NR

cycloheximide and

sodium tungstate and it appears that the possible actions of Pb +2 and BAP is at the R.P.,

level

of

Maheshwari,

synthesis

R.

and

of

the

enzyme

Dabas,

S.,

unpublished

nitrate reductase activity mM)

in

the

maize

leaf

protein

(Sinha

et

cell

results).

(NRA) was significantly

segments

in the

al.,

(Singh,

Induction

inhibited by Pb +2 1994).

Among

of

(0.5

various

divalent cations Ca +2, Mg +2, Mn +2, Zn +2 and Cu +2, only Mn +2 to some extent negated the inhibitory effect of Pb +2 on both in in vivo and in vitro NR activity in maize leaves. Out of various growth regulators viz.,

IAA, GA3,

kinetin

effect

and

Pb +2. Thus,

salicylic

acid,

only

salicylic

acid

negated

toxic

be ameliorated by Mn +2 and salicylic acid and CaCl 2 (Kumar et al., unpublished results).

1993,

(Sinha et al.,

Singh, R.P., Maheshwari,

1994) and K2HPO 4 R. and Dabas,

where

in vivo NR

activity

activity is either inhibited, 1988a,b;

Kumar et al.,

1994b).

It

activity, the cases.

may

be

S.,

The response of NR activity to lead is different if

enzyme is assayed by in vivo and in vitro methods as reported cases

of

it was demonstrated that toxicity of Pb +2 on NR activity could

1993;

related

is generally

inhibited,

unaffected or even increased Bharti to

and Singh,

restricted

1993,

NADH

1994;

supply

in several

in vitro

enzyme

(Sinha et al., Singh et al., to

the

enzyme

as in general in vivo enzyme inhibition was observed in most of A direct

regulatory

role

of the metal

to the in vitro enzyme

activity which is dependent on some other factors may be likely.

Further,

Pb caused inhibition of root NR activity in a comparatively lead tolerant

2477 sesame

cultivar

(PB I) got

with the metal. Whereas, additive

abolished

at saline

level

of NaCl,

the same salinity level caused by NaCl showed an

inhibition to root NR activity of mungbean seedlings

Singh,

1994;

Sinha,

S.K.

if added

Singh et at., and Tripathi,

1994b; R.D.,

Singh,

R.P.,

unpublished

Dabas,

(Bharti and

S., Chaudhury,

results).

A.,

The NR inhibition

in the presence of Pb may be due to: i) The reduced supply of NADH due to its oxidation by lead or its reduced production

due

1993).(ii)

The

because Boyer,

to

swelling

lesser

NO 3

of

the

supply

mitochondria

to

the

site

(Gangenbach

of

the

lead treatment can create water stress to the plants 1976;

Burzynski

and

Jakob,

1983;

Burzynski

et

enzyme

(Shaner and

and Grabowski,

(iii) A reduced synthesis of NR protein due to Pb +2 supply Maheshwari, R. and Dabas, S., unpublished results).

al.,

synthesis 1984).

(Singh, R.P.,

(iv) A possible direct

effect on the enzyme as the metal has a high binding efficiency with -SH groups (Prasad and Prasad, 1987). Glutamine synthetase in soybean leaves is also inhibited by 100 mg pb+2g -1 (Lee

et

al.,

1976).

Manisha,

1991)

to

effect

its

regulation

on

been

found

nitrogenase

the

n/f

nitrogenase

enzymes,

e.g.,

mungben

nodules

Glutamate

has

in

Nostoc

muscorum

activity

gene.

possibly

Negative

effects

through

of

the

have

synthetase

also

dehydrogenase

Dabas

nitrogen

of

et

organic

al.,

young

metal supply

been

activity

and

L-glutamate

demonstrated of young

(Dabas

negative on

mungbean

dehydrogenase and

roots

1995).

Total

seedlings

soluble

increased

in

protein roots

Singh,

the

and

and

and

in

1994).

leaves

and

(Dabas and Singh, total

shoots

of

cotyledon

has

indicated

that

lead

organic

during

causes

translocation of the reserve to the growing roots and shoots aged

a

metal

the

(Dabas et at., 1995). A corresponding decrease in the total

nitrogen

see Table

and

activity and the activity of ammonia assimilating

glutamine

also in the root nodules have increased to some extent 1994~

(Trehan

that lead diminished capacity of alga to fix nitrogen due

of

nodulation,

It

a

higher

(Dabas, 1992,

3). Lead exposure decrease the organic nitrogen content of the

seedlings,

possibly

because

of

reduced

synthesis

of

nitrogenous

compounds in the plant parts (Sinha et al., 1988a, b). MECHAIIISII OF TOI2~IAIICE

A common reaction of plants to metal stress is the induction of peroxidase (POD).

POD induction has been noticed

Glycine (Lee

max

et

hypothesized including (H202,

and

al., as

heavy

hydroxyl

reactive.

in Medlcago 1976;

These

a

Maier, general

metals.

radicals

and

in leaves

1978a,b). reaction

During

and super

thylakoid membranes

sativa

in response to Pb +2 in leaves of

oxide

such

Activation during

stress

radical)

intricate

of

several

intermediary

are generated

lipid

(Elstner and Osswald,

and roots

peroxidation

1984).

of gea mays

oxygen kinds forms

has of

been stress

of oxygen

which

are highly

and

destabilize

247'8 Table

Total

~.

parts

Plant species

soluble during

Plant parts

Roots Leaves

Vigna radiata L. cv. Pusa Baisakhi

Root Nodules Roots Shoot Cotyledon

cv. ML-337

Roots Leaves

Zea mays Leaves cv. Ganga Safed 2

nitrogen

content

in

plant

Total soluble protein (mg. p r o t e i n g-I fr.wt)

Total organic nitrogen (mglnitrogen g-~ fr.wt)

14

9.74±0.44 10.25±0.90

5.18±0.79 4.64±0.99

Sinha,

5

1.73±0.04 2.53±0.06 4.79±0.13 8.26±0.26

1.37±0.20 2.20±0.07 ND ND

Kumar 1993 Kumar 1993

et al.

0.0 0.5 0.0 0.5

PB-I

organic

Age of the plant (days)

0.0 1.0

Sesamum Roots indicum L. cv. HT-I Leaves

and

Pb +2 supply.

Lead supplied (mM)

Pisum Leaves sativum L. cv.Aranchal

cv°

protein

5

0.0 i°0 0.0 1.0

5

0.0 1.0 0.0 1.0 0.0 1.0 0.0 1.0

34

0.0 1.0 0.0

5

et al.

1.2±0.034 2.6±0.033 3.5±0.103 3.5±0.187

Bharti Singh, Bharti Singh,

and 1993 and 1993

3.40±0.04 2.21±0.05 ND ND ND ND ND ND

7.50±0.38 7.03±1.01 2.58±0.10 2.35±0.08 3.12±0.09 3.80±0.06 3.15±0.07 2.93±0.08

Dabas,

1992

Dabas,

1992

Dabas,

1992

Dabas,

1992

ND ND ND

2.70±0.02 2.95±0.02 4.91±0.32

Singh et al. 1994 Singh et al. 1994

12.80±2.02 12.15±1.17

2.01±0.30 2.18±0.20

Singh,

5 5 5

5

14

1988b

ND ND ND ND

5

0.0 1.0

References

1988a

ND= Not determined.

Quenching

of

preservation in s y m p l a s t mays

to

appears A

inside

Pb +2

that

lead.

Though

i)

of the

during

survey

H202

cell. stress

there

Some

the

is,

therefore,

of b i o l o g i c a l

is

are

exact

a

membranes Like

et

difference

mechanism

in

to of

al., the

even

lead

mechanism

lead and o t h e r

peroxidase,

(Hoxa

tolerant

protection

when

catalase 1985).

It

response very

tolerance

for

is also

induced from

species

and

concentration

is not

fully

the

accumulate

appears

of

high

metals

in Zea

tolerance varieties of

metal.

understood,

it

that: differential the

tissue

and e n d o d e r m i s

act

accumulation

occurs as a

e.g.

in

barrier

and maize

compartmentalization roots,

and keeps

the

cells

of of

the

inner

metal cortex

lead away from the p r o c a m b i u m

2479 T a b l e 4.

M e c h a n i s m of Lead t o l e r a n c e in plants.

Strategies involved

Tissue and details

References

i.

Lead tolerance is controlled by fewer genes

In Fescuna ovina Pb tolerance is transmitted to seed progeny.

Urquahart,

2.

Inducible lead tolerance

High lead tolerance in Silene inflata population correlated with high Castatus and high tolerance to Ca-deficit.

Antosiewicz, 1995

3.

Inherent constitutional lead tolerance

Tolerance characterized by high Ca status in tomato

Antosiewicz, 1993

4.

Calcium mediated lead tolerance towards photosynthesis

CaCI 2 could protect Pb +2 inhibition in Photosystem II

Rashid and Popovic, 1990

5.

Phytochelatin induction as lead detoxifying mechanism

In cell suspension culture of Rauwolfia serpentina PC2, PC 3 and PC 4 were identified

Grill et al., 1987 Grill, 1989

Hydrilla verticillata produces PC 2 and PC~ and few unidentified thlol as Pb detoxifying agents.

Gupta et al., 1995

Majority of Pb is deposited in apoplast and vacuole in Anthoxanthum odoratum and moss Bryum argentum.

Qureshi et al., 1986 Shaw and Albright, 1990

ii. Lead localized in the cell walls and nuclei of absorbing roots.

Hammett,

iii. Lead tolerance correlated with Pb chelated to cell wall in Anthoxanthum odoratum.

Poulter et al., 1985

iv. Lead was bound to orthophosphate in the nucleolus of onion root tips.

Tandler and Solari, 1969

v. Lead is often found in the symplast of the cells associated with electron fuse precipitate localized in membranous inclusions, vesicles or organelles.

Koeppe,

vi. Lead was deposited in dictyosome vesicles. Pb was also deposited in the cell wall outside plasmalemma.

Carl et al., 1974

6.

Compartmentalization in different organelles

1971

1928

1981

2480 Table

4 continued

7.

Reduced uptake plants

(Wierzbicka, observed

1987).

than may

inducible

tolerance

be

(Antonovics

et

al.,

alterations occur

Ca,

can

where

ecotypes, studies

to

Pb can

Hevesy, 1923, Malone et al., 1974

v. The CaCO 3 added to nutrient solution decreased the concentration of lead in leaves, stem and roots of Barley & Bush bean.

Patel et al., 1977

vi. In the soil grown rye grass, the roots restrict the m o v e m e n t of lead in the root tips of high yielding plants.

Jones et al., 1973

accumulate and

the

more

lead

and,

therefore,

specific

in

plants Baker,

with

with

metal

through This

Some

1991).

various

Thus,

cellular

interference

can

protein

these

to

a

summarized

fight

ecotype. with

binds

have

either

in Table 4.

weight

and

been

(iii) Metals

toxicity

molecular

which

involving

can

tolerance

(ii)

in

the

can

be

A

desired

plant

in

cysteine

inactivates

depicted

inducible

various

processes

in

the Fig.

rich toxic I.

or constitutional

and Ca

involving

be of a lower

ways.

level

if any,

will be

synthesis

of

plants

polypeptide, metal.

in

Further

Tolerant

Various

cell

transported

Pb tolerance

may stimulate

have

Baker et

to Ca deficit and in those with high Ca status.

low

peptides

species

1987;

metal

1994).

Lead

the

physiological

plants

(Baker,

systems

toxicity.

(Tomsing and Suzkvi,

interfere.

Mehrag,

metabolic

1986

of

the

constitutional

1987;

various

most

tissue.

uptake of toxic metals

the

counter

leaves

to

to

in a specific

phytochelatin, plants

iv. Lead is bound to roots and such binding serves to protect upper plant parts from lead injury.

are needed to verify which of above possibilities,

synthesize of

Bassuk,

be correlated

tolerant

operational stress

iii. Different type of organic matter reduced the uptake of Pb in lettuce plants.

1971; in

through Ca channels metabolism

John & Laerhaven,

limiting

contrast

to

ii. Application of lime and low level of N repressed the uptake of added lead in Letuca sativa and Avena Sativa.

different

in

seems

Singh et al., 1994a.

shoot

1989)

shift/

i. Lead augmentation was reduced in presence of K2HPO4, CaCI 2 and KNO 3 in Vigna radiata.

Roots

the

responses

al.,

in

the

Biosynthesis strategies

Pb tolerance

of

have been

2481

LEAD

oo

•

Z,

GLYCINE

% % GLUTATHIONE

~

CYSTEINE

$ $ | '~-GLYTAIMYLCYSTEINE I SUBSTRATES

Figure

I.

class

Higher

III

concentrations

of

Phytochelatins major

is

vacuole

and

lead in

complex

supposed

to

plant

or

or

(Poly (TEC~

precursor

intracellular metal

plants

metallothioneins

cell

suspension

phytochelatins

other

heavy

cultures

when

metals

synthesize

exposed (Cu +2 ,

to

higher

Cd +2 ,

Zn+2).

G-peptides are synthesized from glutathione as

the

presence

formed

by

detoxify

(Based on Steffens,

of

phytochelatin

phytochelatin the

metal

1990; Rauser,

with

possibly

synthase.

lead by

or

The

other

heavy

sequestration

into

1990;Salt and Rauser,1995 Meuwly

et al.,

1995; Grill et al.,

1987,

et al.,

1992; Gupta et al.,

1995 Mehra et ai.1995;

1989; Robinson et al.,

1993; De Knecht

Tripathi et al.,

1996

a,b). Nature has evolved at least two different mechanism for detoxifying heavy metals

including

cyanobacteria mustard

Pb +2

(blue

in which

in

green

heavy

vertebrates, algae)

metals

and

are

invertebrates, higher

complexed

plants by

some

like

fungi,a

wheat,

metallothioneins

few

barley, (MTs).

These include low molecular weight cysteine rich proteins chelating heavy metals

viz.

thiolate

transcriptional

coordination.

These

proteins

are

induced

at

level by the same metal to which the proteins bind. These

MTs are known to detoxify by complexing with heavy metal ions. On the other hand, higher

plants

an unique metal

and algae

(Grill et

detoxification al.,

1985,

system has

Gekeler

et al.,

evolved 1989)

in and

2482 some fungi

et

al.,

1986)

r(Glu-cys~

where

-Gly,

constitutive

cysteine

(n= 2-11),

metal detoxification.

Rauser, etc.

detoxify 1990)

can

peptides

of

the phytochelatins

phytochelatin the

and

in

(Kneer and Zenk, 1992). Zn +2

rich

Mehra et al.,

1984;

the

(PCs)

1988 Grill

general

are

structure

involved

in the

These are produced by the action of metal activated

enzymes,

Phytochelatins 1990;

(Kondo et al.,

including yeast

serve

metals doing

synthase by

so,

et

(Grill

thiolate

al.,

coordination

reactivate

metal

1989).

(Steffens,

poisoned

enzymes

PCs when complexed with essential ions like Cu +2,

homeostatic

function

by

interacting

with

(Grill et al.,

and resulting in functional metalloenzymes

apoenzymes

1991, Thuman et

al., 1991.) However,

(Robinson et al.,

a survey of literature on phytometallothioneins

1993) and PCs (Grill et al.,

1989; Grill et al.,

1987) reveal that PCs and

not MTs are the major metal detoxification system of higher plants. Recent reports

have

produces 1994),

suggested

both

Pcs

although

(Mehra

et

that

(Howden both

al.

these

1988).

phytometallothionein

during

et al.

stress

1995),

of

and

detoxifications

Cadmium,

Cu +2

(Zhou

system and

Rauwolfia

of

yeast

produced

1993).

However,

et

(Grill

in

stress

There

Pb (i000 ~M)

(PC2, PC 3 and PC4)

serpentina

thaliana

Goldsbrough,

coexisted

(Robinson et al.,

in many crop plants

has been found to induce synthesis of PCs culture

and

Zn +2

are no reports of Pb inducing phytometallothioneins. suspension

Arabidopsis

Cd,

Mts

al.,

in the cell 1987).

Lead

also induced synthesis of phytochelatin peptides in a submerged macrophyte

Hydrilla

verticillata

and

this

was

accompanied

by

a

reduction

in

the

cellular glutathione levels in the plant (Gupta et al., 1995). The

PCs

in

response

to

Rhyncostegium riparoides at

sites

influenced

contamination. of

metal

(Jackson et al., in

the not

However,

supply

Cd +2

and

Pb +2

metal

contamination

of Zn +2,

Cu +2 and Cd +2

these

were

investigated

in

were

absent

as

well

as

induced the

free

of

formation

in Pb +2 contaminated

moss

1991).The use of X-ray photoelectron spectroscopic method of

lead

in

endiviifolia

bound

(Soma et al.,

Cu +2,

heavy

complexes,

analysis

ludwigii,Pellia was

by

While

binding

Zn +2,

a wide spread moss in flowing waters which occurs

to

sulphur

1988;

in Pohlia

some

bryophytic

and Scapania but

distributed

Shaw et al.,

ludwigii

1987)

evidence

species

as

undulata showed that in

homogenous

in

Pohlia

most of Pb

bonding

states

presumably also in the cell wall. was

presented

for

some

produced

in animal

cells.

bonding

to

sulphate and sulphide. Lead

could

bind

metallothioneins

to

Zn thioneins

could

(Goering and Fowler, denydratase activities

extract

Pb +2

from

Pb

poisoned

Further

ALA

these

dehydratase

1987). Pb +2 has been found to inhibit ALA in mung bean seedlings (Prasad a n d Prasad, 1987).

2483 As

PCs

worth

could

reactive

while

to

study

many the

-SH role

rich of

metal

PCs

poisoned

in

enzymes,

reactivating

Pb

it may

poisoned

be ALA

dehydratase and some other Pb sensitive enzymes in plants. As such studies on the formation of phytometallothioneins and PCs in response to Pb stress are needed particularly from structural and functional view point. SI~01ARYANDC~)NC~USION

The literature available on impact of Pb +2 in the environment demonstrate that the plants are responsive to the metal. The accumulation of the metal in the plant organs and the consequent effects, however, vary according to the species,

concentration of the metal and soil or nutrient composition.

Normally when organic matter, minerals, salts

containing

phosphates

and

certain inorganic salts especially

potassium,

and

lime

are

in

abundant

supply, lead toxicity is not severe and it seems to be reversible with the amendments of nutrient salts of potassium,

phosphate and nitrogen in a few

cases. Toxic levels of Pb affect plant processes at physiological and biochemical levels.

As

the

macromolecules,

metal the

reacts

activity

with

of

important

several

functional

enzymes

is

groups

influenced,

in

some

of

tolerance

in

which are important in photosynthesis and nitrogen metabolism.

Research some

has

identified

plants,

but

process/steps responses

of

to

gene systems

several

important

is

model

there tolerance

lead

has

is complex

in the plant.

no

been

determined.

phenomenon

Thus,

aspects species and,

is

of metal in

which

the

It

appears

controlled

entire

that

plant

by multiple

a better understanding of the knowledge

is required to handle the acute problem of increasing lead toxicity to the plants

and

aspects

human

life.

of tolerance

Efforts

to

are required.

coordinate In addition

research

to

t o provide

address

all

the necessary

data for the production of models that will accurately predict the impact of certain

Pb related

industrial

activities

on plant

life,

the

study of

metal tolerance may also provide methods to detoxify Pb contaminated soils through the use of Pb accumulating

species.

As such the pathway of lead

detoxification in plants needs to be studied in depth.

ACENO~DG~4ENTS

Thanks Research

are

due

to

Institute,

encouragements.

Dr.

P.

V.

Lucknow,

Sane, India

FNA, for

Director,

National

necessary

Botanical

facilities

and

2484 REFERENCES

Ahlbereg, J., Ramah, C. & Wachtmeister, be genetically active. Ambio. Akhter,

M.S.

and Madany,

I.M.

C.A. Organ lead compounds shown to

I: 29-31

Heavy metals

Bahrain. Water, Air & Soil Pollut. Antonovics,

J.,

Bradshaw,

A.D.

and

to

D.M.

their

Mineral

in street

66:111-119

Turner,

plants. Adv. Ecol. Res.. 7 : 1 - 8 5 Antosiewcz,

(1972).

R.G.Heavy

dust

in

metal

tolerance

in

(1971).

status of dicotyledonous

constitutional

and house

(1993).

tolerance

to

crop plants

lead.

Environ.

in relation

Exp.

Bot..

33:

375-589 (1993). Antosiewicz,

D.M.

The

relationship

between

constitutional

and

inducible

Pb-tolerance and tolerance to mineral deficit in Biscutella laevigata and Silene inflata. Environ. Exp. Bot.. Baker, A.J.M. Metal tolerance, New Phytol. Baker,

A.J.M.

metals

and Walker, and

the

Bioavailability. Barker,

W.G.

system

Physiological

quantification

responses of plants to heavy

of

tolerance

and

toxicity.

zinc

in tissue

i: 7-17 (1989).

Toxicity

culture

P.L.

35(1): 55-69 (1995).

106 (Suppl.): 93-111 (1987).

level

of

Bot. 5 0 : 9 7 3 - 9 7 6

of mercury,

cauliflower,

lead,

lettuce,

copper potato

and and

carrot.

Can.

J.

(1972).

Bassuk, N.L. Reducing lead uptake in lettuce. Hort. Science 21(4): 993-995 (1986). Baumhardt,

G.R.

&

Welch,

L.F.

Lead

uptake

and

corn

growth

with

soil

applied lead. J. Environ. Qual., 92-94 (1972). Bazzaz,

F.A.,

Carlson,

R.W.

and

Rolfe,

G.L.

The

inhibition

sunflower photosynthesis by lead. physiol. Plant. Bazzaz,

F.A.,

soyben

Rolfe,

G.L.

photosynthesis

& Windle, to

P.

of

corn

34:326-329

and

(1975).

Differing sensitivity of corn and

lead contamination.

J.

Environ.

Qual.

156-

158 (1974). Bazzaz,

M.B.

and

Govindjee,

reaction. Environ. Lett.: Bhandal,

I.S.

vivo

& Kaur,

nitrate

Effect

of

H. Heavy metal

reductase

Indian J. Plant Physiol.

lead

chloride

on

chloroplast

175-191 (1974). in

inhibition of nitrate uptake and in

roots

of

35:281-284

wheat

(Triticum

aestivum

Bharti, N. and Singh, R.P. Growth and nitrate reduction by S e s a ~ m cv

PB-I

respond

differentially

to

L.).

(1992). lead.

phytochemistry

33:

indicum 531-534

(1993). Bharti,

N.

and

Singh,

differential accumulation

R.P.

heavy and

phytochemistry.

Antagonistic

metal

nitrate

effect

of

toxicity

regarding

assimilation

in Sesamum

35(5): 1157-1161

(1994).

sodium

chloride

biomass indicum

to

biomass seedlings.

2485 Broyer,

T.C., Johnson,

C.M.

and Paull,

R.E.

nutrition. Plant and Soil. 2 : 3 0 1 - 1 3 Brackup,

I.

and

pollutants

Capone.

on

The

nitrogen

effects

fixation

Some aspects of lead in plant

(1972). of

several

(acetylene

metals

and

reduction)

by

rhizomes of Zostera marina L. Environ. Exp. Bet. 25:145-151 Bradshaw,

A.D.

Population

poisoning. Nature. Bradshaw,

A.D.

of Agrostis

169:1098

and Mc Neilly,

tenuis

resistant

to

organic

roots

and

(1985).

lead

and

zinc

(1952).

T.

Evolution

and Pollution,

Edward Arnold,

London (1981). Burzynski,

M. Influence of lead on the chlorophyll

content and on initial

steps on its synthesis in greening cucumber seedlings. Poll. 5 4 : 9 5 - 1 0 5 Burzynski,

(1985).

M. and Grabowaski,

reduction

Acta Soc. Bet.

in

cucumber

and

Jakob,

A.

Influence

seedlings.

of lead on nitrate

Acta

Soc.

Bet.

uptake

Poll.

53:

and

77-86

(1984). Burzynski,

M.

M.

Influence

of

lead

elongation. Acta Soc. Bet. Poll. 5 2 : 2 3 1 - 2 3 9 Cannon,

H.L.

and

Bowles,

lead. Science. Carl,

M.,

Koeppe,

J.M.

Contamination

137:765-766 D.E.

R.W.,

and Miller,

Stukel,

Contamination Reinbold,

by

J.J.

lead

eds.)

auxin

induced

cell

(1983).

of vegetation

by

tetraethyl

(1962). R.J.

by corn plants. Plant Physiol. Carlson,

on

and

heavy

for

of

lead accumulated

(1974).

Bazzaz,

and other

Institute

Localization

53:388-394

F.A.

metals

In:

(G.L.

Environmental

Environmental KRolfe

and

Studies,

K.A.

Urbana,

Illinois, pp. 51-66 (1977). Chandra,

P., Tripathi,

and

amelioration

R.D., Rai, U.N., Sinha, of

non

point

source

S. & Garg, P. Biomonitoring pollution

on

some

aquatic

bodies, Water Sci. Tech., 38 (3/8): 323-326 (1993). Chow, T.J. Lead accumulation in road side soil and grass. Nature 225: 295296 ( 1 9 7 0 ) . Cox,

W.J.

and

Rains,

D.W.

Effect

of

lime

on

lead

uptake

by

five

plant

species. J. Environ. Qual. i: 167-169 (1972). Dabas, S. Ph.D. Thesis, Deptt. of Biosciences, M.D. India (1992). De

Knecht,

J.A.,

Evidence increased Phytol. Ei-Hussanin,

Koevoets,

against

a

cadmium

P.L.M.,

role

for

tolerance

122:681-688

(1992).

A.S.,

T.M.

contamination

Labib,

Verkleij,

J.A.C.

phytochelations in Silene

in

vulgaris

and Dobal, A.T.

E.F.

and

Osswald,

naturwiss. Rundschau.

W.

Elchtenterhen

37x 52-61 (1984).

Ernst,

(Moench)

Potential

of sandy soils after different

New

Zn and B

periods with

66:239-249

in

W.B.O. selected

Garcke

Pb, Cd,

irrigation

sewage effluent. Water, Air and Soil Pollution. Elstner,

and

naturally

Reinluff

(1993). gehleten.

2486 Fiussello, N. and Molinari, 1 9 : 8 9 - 9 6 (1973). Forstner,

U.

and

Wittman,

springer-verlag Gekeler,

W.,

M.T. Effect of lead on plant growth. G.T.

Metal

pollution

Berlin, Heidelberg,

Grill,

E.

Winnacker,

in

aquatic

Allionia

environment,

New York (1979).

E.L.

and

Zenk,

M.H.

Survey

of

plant

kingdom for the ability to bind heavy metals through phytochelatin naturforsch. 4 4 : 3 6 1 - 3 6 9 (1989). Gengenbach, toxin

B.G., Miller, from

mitochondria Goering,

P.L.

Biophys.

Koeppe,

Fowler,

acid

B.A.

Kidney

dehydratase

E.,

(race

T)

253(1):

by

C.J. The effect of on

isolated

corn

(1973).

Zinc-thionein

inhibition

regula£ion

lead.

Arch.

et

of amino Biochem.

48-55 (1987).

Goldsmith, C.D. Jr. Scanion, P.F. Toxicol. 16(1): 66-70 (1976). Grill

D.E., Arntzen,

maydis

swelling. Can. J. Bot. 51:2119-2125

and

levulinic

R.J.,

helminthosperium

Z.

Winnacker,

E.L.

heavy metal complexing

and

& Pirie,

Zenk,

peptides

M.H.

W.R.

Bull.

Environ.

Phytochelatins:

of higher plants.

the

Science.

Cont.

principal 230:

674-

676 (1985).

Grill

E. Phytochelatins Biology

in plants.

In: Metal

ed.

Hamer,

and Chemistry.

York, Alan R. Liss, Inc. Grill

Grill

D.H.

Ion Homeostasis:

D.R.

Winge,

pp.

Molecular

283-300

New

(1989).

E., Winnacker, E.L. and Zenk, M.H. Phytochelatins: a class of heavy metals binding peptides from plants, are func£ionally analogous to metallothioneins. E., Winnacker,

Proc. Natl. Acad. Sci. USA, 84:439-443

E.L.

heavy metal complexing

and

Zenk,

peptides

M.H.

Phytochelatins:

of higher plants.

(1987). the principal

Science.

370:

674-

676 (1985). Grill

Grill

E., Gekeler, W., Winnacker, E.L. and Zenk, M.H. Homophytochelatins are heavy metal binding peptides of homogluta-thione containing Fables. FEBS Lett., 2 0 5 : 4 7 - 5 0 (1986). E., Loffler, Winnacker, E.L. and Zenk, heavy

metal

glutathion

by

(Phytochelatin

binding

peptides

specific synthase).

of

r-glutamylcystene Proc.

Natl.

(1989). Grill, E., Winnacker, E.L. and Zenk, M.H. Enzymology. Vol. 205:333-341 (1991).

M.H.

plants

are

Phytochelatin,

the

synthesized

from

dipeptidyl

Acad.

Sci.

USA.

Phytochelatins,

transpeptidase 86:

6838-6842

In:Methods

Guilizzoni, P. The role of heavy metals and toxic materials in physiological ecology of submerged macrophytes. Aquatic Botany.

in

the 41:

87-109 (1991).

Gupta, M. and Chandra, P. Lead contamination Hydrilla verticillata (L.F.) Rogle. J. 29(3): 503-516 (1994).

in Vallisnaria Environ. Sci.

spiralis &

Health.

and A

2487 Gupta,

M., Rai, U.N.,

in

Tripathi,

glutathione

Chemosphere. Hammett,

F.S.

and

R.D.

and Chandra,

phytochelatin

R.,

Studies in the biology of the metal. Ziegler,

14C02

fixation

Biochem. Heresy,

G.

H.

and

and

on

the

synthesis

to

the

ATP

The

effect

164:126-134

and

of

of

by

lead

ions

spinach

on

the

chloroplast.

(1973) .

translocation

application

I. The localization of

(1928).

I.

absorption

contribution

4:183-186

Ziegler,

Physiol. Pflanzen. The

verticillata.

30(10): 2011-2020 (1995).

lead growing roots. Protoplasma. Hamppe,

P. Lead induced changes

hydrilla

in

of

the

lead

method

by of

plants.

A

radio-active

indicators in the investigation of the change of substance in plants.

Biochem. J.. 1 7 : 4 3 9 - 4 4 5 Howden,

R.,

Goldsbrouqh,

sensitive

cad

1

(1923).

P.B.,

mutants

deficient. Plant Physiol. Hoxha,

¥., Jablanavic,

in

the

plant

Anderson,

of

to

C.¥.,

Bazzaz,

F.A.

K. & Filipovic,

& Vanderhoef,

P.P.,

complexes to

Robinson,

N.J.

L.N.

& Whitton,

elevated

concentration

of

Jana,

S. on

& Chaudhury, senescence

Pollut. Jana,

S.,

in

on

heavy

The

inhibition

54:122-124 B.A.

T.

Acta

of

soybean

(1974).

Low molecular weight metal

Cd +2 ,

riparioides

Cu +2 ,

exposed

Pb +2 ,

in

the

effect

aquatic

of heavy metals

and

Soil

of

heavy

Pollut.

33:

23-27

Metalliferous

mine

spoil

plants,

Water,

pollutants

Air

(1984).

&

Cuscuta

Zn +2 ,

metals.

Exp. Bot. 31(3): 359-66 (1991).

Synergistic

submerged

21:351-357

Dalal,

metal

M.A.

Cadmium

Phytochelatin

(1985).

in the fresh water moss Rhynchostegium

laboratory and field. Environ.

C.S.

are

R. Catalase activity

with

i0:21-24

m e t a b o l i s m by Cd & Pb, Plant Physiol., Jackson,

Cobbett,

(1995).

contamination

Biologica et Medica Experimentalis. Huang,

&

thaliara

107:1057-1066

M., Abdullai,

exposed

C.R.

Arabidopsis

Barua,

B.

reflexa.

Effect

Water

and

Air

relative

and

Soil

toxicity

(1987). John,

M.K.

& Van-Laerhoven,

C.

Revegetation

contaminated by Pb & Zn. Environ. John, M.K. & Van-Laerhoven, by lime,

nitrogen

of

Pollut.

i00:163-173

(1976).

C. Lead uptake by Lettuce and Oats as affected

& source of

lead.

J. Environ.

Qual.

1(2):

169-171

(1972). Johnson, mine

M.S, soil

Me Neilly,

T & Putwain,

contaminated

by

P.O.

lead and

Revegetation of metalliferous

zinc.

Environ

Pollut.

12:261-277

(1977) Johnson, from

W.R. two

(1977).

& Proctor,

J. A compaative study of metal

constrasting

lead

mine

sites.

Plant

leaves

Soil.

46:

in plants 251-257

2488 Jones,

L.H.P.,

Jarvis,

Perennial

Ryegrass

S.C. and

&

Cowling,

R.E.,

Bettany,

J.R.

38:605-619

& Stewart,

J.W.B.

applied lead by alfalfa and brome-grass 56:485-494 Kneer,

R.

&

N.,

Imaik,

Hayashi,

Y.

M.H.

Phytochelatin

Isabe,

Grooke,

tissues

of

M.,

induced

W.M.

higher

content. Nature, Krishnayappa, Cassia

soil

by

(1973). Can.

J.

Soil

Sci.

protect

plant

Goto,

T.,

Murasugi,

plants

192: 142-143,

N.S.R.

tora

lower

& Bedi,

and Cassia

R.H.E.

S.J.

A.,

peptides

in a fission yeast

& Inkoson, and

enzymes

from

heavy

31(8): 2663-2667 (1992).

structures and synthesis. Tetrahedran Lett. A.,

from

The uptake of native and

from soil.

Cadystin A and B major unit

binding peptides Kought,

uptake

(1976).

Zenk,

metalpoisoning. Phytochemistry. Kondo,

Lead

its relation to the supply of an essentially

element (Sulphur). Plant and Soil Karamanos,

D.W.

separation,

3869-3872

Cation and

Wakerda,

comprising

C.

revision

of

(1984).

exchange capacities

their

&

cadmium

related

uronic

at

acid

(1961). Effect of automobile

occidentalis

L.

Environ.

lead pollution 40:

Pollut.

of

221-226

(1986). Koeppe,

D.E.

Lead:

In: Effect metals

on plant

Metal

function,

the

Minimal

Pollution

ed.

N.W.

Toxicity

Lepp.

of

WI.

on Plants.

Applied

Lead

in Plants

I. Effects trace

Science

Publisher,

pp. 55-76 (1981).

London.

Kuhad,

Understanding

of Heavy

M.S.

&

Malik,

R.S.

Source:

Department

of

soil

science,

C.S.A.

Uniersity, Hissar, India (1989). Kumar,

G.,

Singh,

production

in

R.P.

&

Sushila.

Sesamum

indicum

Nitrate L.

environment. Water, Air & Soil Pollut. Lagerwerff,

J.V., Armiger,

W.H.

from soil and air. Soil Sci. Lane,

S.D.,

Margin,

E.S.

assimilation

seedlings

66:163-171

a

J. Environ.

W.C.

Qual.

biomass enriched

(1993).

115:455-460

& Carrod,

J.F.

(1973).

Lead

B.A., Chung, K.H.,

toxic

effect

144:7984

Paulson, G.M.

on

Indole-3-

(1978).

& Laing, G.H. Lead

effect on several enzymes and nitrogenous compounds Lierohardt,

and

lead

& A.W. Uptake of lead by alfalfa and corn

acetic acid induced cell elongation. Planta. Lee, K.C., Cunningham,

in

in soybean

leaf.

357-359 (1976).

& Koske,

T.J.

The lead content of various plant species

as affected by cycle-littume humus.

Commun.

Soil

Sci.

Plant

Anal.

5:

85-92 (1974). Maheshwari,

R.

M.

Phil.

Dissertation,

Department

of

Biosciences,

M.D.

University, Rohtak, Haryana (1993). Maier, R. Aktivitat und multiple formen der peroxidase in unverbleiten und vrbleiten pflanzen von Zea mays (1978a).

and Medico

sativa,

Phyton.

19:83-96

2489 Maier,

R. Studies on the effect of lead on Acid Phosphatase

Z. Pflanzenphysiol. Malone,

C.D.,

Koeppe,

87:347-54

D.E.

& Miler,

R.J.

by corn plants. Plant Physiol. Martin,

G.C.

& Hammand,

P.B.

Mehra,

R.K. Tarbet,

Localization of Pb accumulated

53:388-394

(1974).

Lead uptake by bromegrass

soil. Agron. J., 5 8 : 5 5 3 - 5 5 4

& Winge,

D.R. Metal specific synthesis

and r-glutamyl

peptides

Proc. Natl. Acad. Sci. USA, 85: 8815-8818, Mehra, R.K., Kodati, V.R. co-ordination

in

from contaminated

(1966).

E.B., GrayW.R.

of two metallothioneins

in Zea mays.

(1978b).

and Abdullah,

in Candida

glabrata.

(1988).

R. Chain length dependent Pb (II)

Phytochelatins.

Biochem

Biophys.

Res.

Comm.

215:

730-736 (1995). Meharg,

A.A.

Integrated

tolerance

mechanisms:

Constitutive

plant responses to elevated metal concentrations Plant Cell & Environ. Miles,

C.D.,

Brandle,

Uhlick,

D.J.

17:989-993

J.R.,

lead. Plant Physiol. Meuwly,

P.,

thiol

Thibault, peptides

D.J.,

Schwan,

induced

Chuder,

Photosystem

49:820-825

P.,

are

of

adaptive

(1994).

Daniel,

Inhibition

and

in the environment.

II

O.,

Schnare,

isolated

P.O.

&

chloroplast

by

(1972).

A.L.

by

& Rause,

cadmium

W.E.

in maize,

Three The

families

Plant

of

Journal

7(3): 391-400 (1995). Miller,

J.E.,

Hassat,

and extractable

J.J.

J.E.,

surption Miller,

6:339-347

Hasset,

J.J.

capacity

Plant Annal.

D.E.

The effect of soil properties

lead levels on lead uptake by soybean.

Sci. Plant Annal. Miller,

& Koeppe,

&

Koeppe,

on the uptake

6:349-358

J.E., Hasset, J.J.

Commun.

Soil

(1975a). D.E.

of

The

effect

lead by corn.

of

soil

lead

Commun.

Soil

Sci.

(1975b). & Koeppe,

D.E. Interaction of leaf and cadmium

on metal uptake and growth of corn plants. J. Environ.

Qual.

6:18-20

(1977). Morzek, Jr. E. & Funicelli, N.A. Effect of lead ans zinc in germination of Spartina

alterniflora

Bot. 2 2 : 2 3 - 3 2 Motto,

H.L.,

plants;

Daines,

R.H.,

Sci. Technol.

S. & Maitra,

germinating

Chilko,

W.E.

at various

salinities.

Environ.

Exp.

D.M.

& Motto,

C.K.

Lead in soil

and

rice

4:231-237

(1970).

P. The effect of lead on growth and metabolism of seeds

Exp. Biol., 1 4 : 5 1 9 - 5 2 1 Odum,

seeds

its relationship to traffic valume and proximity to highways.

Environ. Mukherjee,

L.

(1982).

& Drifmeyer,

J.E.

and

on mitosis

of onion

root

tips.

Ind.

J.

(1976). Sorption of pollutants

review. Environ. Health Perspect.

27:133-142

by plant detritus.

(1978).

A

2490 Page, A.L. & Ganje, T.J. Accumulation of lead in soils for regions of high & low motor vehicles traffic density,

Environ.

Sci. Tech.

4: 140-142

(1970). Pahlsson,

A.B.

Toxicity

of

heavy

metals

plants. Water, Air & Soil Pollut. Patel,

P.M.,

Wallace,

phytotoxicity

&

Romney,

lead

A~al. 8 : 7 3 3 - 7 4 0 Prasad, D.D.K.

A.

of

and

(Zn,

E.M.

lead

Cu,

47:287-319 Effect

transport.

R.K.

Pb)

of

to

chelating

Commun.

vascular agents

Soil

Sci.

& Prasad, A.R.K.

Effect of lead and mercury on chlorophyll

& Srivastava,

H.S.

Increase

26:881-883

in RNA

in bean

(1987).

leaves by light

involves a regulator protein. Agric. Biol. Chemo 9 : 2 0 9 9 - 2 1 0 4 Poulter,

A.,

on

Plant

(1977).

synthesis in mung bean seedlings. Phytochem. Puranik,

Cd,

(1989).

Collin,

H.A.,

Thurman,

D.A.

& Hardwick,

K.

(1985).

The role of the

cell wall in the mechanism of lead and zinc tolerance in Anthoxanthum odoratum L. Plant Sci. 4 2 : 6 1 - 6 6 Qureshi,

J.A.,

Hardwich,

K.

(1985).

& Collin,

H.A.

Intracellular

localization

of

lead in a lead tolerant and sensitive clone of Anthoxanthum odoratum. J. PI. Physiol. Rashid,

122:357-364

A. & Popovic,

(1986).

R. Protective role of CaCl 2 against Pb+2

in Photosystem II. FEBS Lett.

271:181-184

Rauser, W.E. Phytochelatins. Ann. Rev. Biochem.

59:61-86

Rebechini,

ultrastructural

H.M.

& Hanzelly,

chloroplast

of

the

L.

Lead

induced

hydrophytes.

Z.

inhibition

(1990). (1990).

Pflanzenphysiol.

changes 73:

in

377-386

(1974). Robinson,

N.J.,

Tommey,

Metallothioneins. Rolfe,

G.L.

& Bazzaz,

A.M.,

295:i-i0 F.A.

Kuske,

Ch.

&

Jackson,

P.J.

Plant

(1993).

Effect of

lead contamination

on transpiration

and photosynthesis of loblolly pine and Autumn olive. Forest Sci.

21:

33-35 ( 1 9 7 5 ) . Rolfe, G.L. & Reinhold, heavy

metals.

K.A. Environmental contamination by lead and other

Inst.

Environ.

Studies,

Urbana,

Illinois,

pp.

143

(1977). Salt,

D.E. Across

& RAuser, the

W.E.

tonoplast

Mg of

ATP-Dependent oat

roots.

Transport

Plant

of

Physiol.

phytochelatins 107:

1293-1301

(1995). Sarkar,

A.

& Jana,

activity

S.

Effect

of Azolla pinnata.

of

combination

Water,

of

heavy

metals

Air and Soil Pollut.

35:

on

hill

141-145

(1987). Scbuck, E.A. & Locke, J.K. R e l a t i o n s h i p o f automotive lead p a r t i c u l a t e s t o certain consumer crops. Environ. Sci. Technol.

4:324-330

(1970).

Sekerka, V. and Bopak, M. Influence of lead on plant cell. Acta Fac. Rerum Nat. Univ. C o ~ e n i a n c e

Physiol. Plant 9 : 1 - 1 2

(1974).

2491 Shaner,

D.L.,

Boyer,

Plant Physiol. Sharpe,

V.

J.S.

Nitrate

58:499-504

& Denny,

reductase

activity

in

maize

leaves.

(1976).

P. Electron microscope

studies on the absorption

and

localization of lead in the leaf tissue of Potamogeton pectinatus.

Exp. Bot. 2 7 : 1 1 5 5 - 1 1 6 2 Shaw,

J.,

Antonovics,

variation

on

(1976).

J.

mosses

J.

&

Anderson,

L.E.

in

tolerance

to

D.L.

Potential

for

Interand

copper

and

intra-specific

Environ.

zinc.

41:

1312-1325 (1987). Shaw,

A.J.

& Albright,

tolerance in Bryum argenteum, diverse population

a mass.

the

evolution

of

heavy

metal

II. Generalized tolerance among

from metalliferous

New Phytol.

areas.

84:

175-188

lead

caused

(1990). Singh,

R.P.,

Maheshwari,

R.

decreased

in

biomass

seedlings

of

K2HPO 4 and

&

Sinha,

S.K.

accumulation CaCI 2.

of

Recovery

mung

Indian

J.

Exp.

of

(Vigna

bean

radiata

Biology.

32:

L.)

507-510

(1994a). Singh, R.P.,

Bharti,

N. a Kumar,

G. Differential toxicity of heavy metals

to growth and nitrate reductase actiity of Sesamum indicum seedlings.

Phytochemistry Sinha,

S.K. Ph.D.

35(5): 1153-1156 (1994b). Thesis,

Deptt.

of Biosciences,

M.D.

University,

Rohtak,

India (1990). Sinha, S.K., srivastava, H.S. & Misra, and

excised

maize

Cont. Toxicol. Sinha,

S.K.,

leaves

in

41:419-426

Srivastava,

H.S.

Nitrate assimilation

S.N. Nitrate assimilation in intact

the

presence

of

Bull.

lead.

Environ.

(1988a). & Mishra,

in pea leaves.

S.N.

Effect

Acta Soc.

of

Bot.

lead

Poll.

on

RNA

57(4):

and 457-

463 (1988b). Sinha,

S.K.,

Srivastava,

regulates

H.S.

and cations

on

& Tripathi, the

R.D.

inhibition

by lead in maize leaves. Bull. Environ.

Influence

of

of

chlorophyll

Cont. Toxicol.

some

growth

biosynthesis

51(2):

241-246

(1993). Sinha,

S.K.,

Srivastava,

regulators

H.S.

divalent

& Tripathi,

cations

on

the

R.D.

Influence

inhibition

activity by lead in maize leaves. Chemosphere Smith,

W.H.

Lead

contamination

of

road

sides

of

of

some

nitrate

growth

reduction

29(8): 1775-78 (1994). white

pines

Forest

Sci.

17(2): 195-198 (1971). Soma,

M.,

Seyama,

H.

&

Satake,

E.

X-ray

photoelectron

spectroscopic

analysis of lead accumulated in aquatic bryophytes. Talanta

35:68-70

(1988). Srikanth,

R.,

Toxicol. Steffens,

Rao,

A.M.,

50:138-143

Kumar,

C.S.

&Khanum,

A. Bull.

Environ.

Contam.

(1973).

J.C. The heavy metals binding peptides of plants. Ann.

Physiol. PI. Mol. Biol. 4 1 : 5 5 3 - 5 7 5

(1990).

Rev.

PI.

2492 Sung,

M.W.

Studies

on

participation

plant growth. Korean J. Bot. Symeonidis,

S.L., Mc-Neilly,

Agrostatis

Tandeler,

lead

ion

cadmium,

A.D.

&

&

copper,

lead

Solari,

A.J.

Nuclear

D.,

Crowdy,

S.H.

The

Srivastava,

J.,

Grill,

H.S.

E.,

& Ormrod,

Winnacker,

requiring apoenzymes 284:66 furo-2

of

D.P.

New

Phytol.

ions-electron (1969).

chelate

2:211-213

Physiological

in

the

(1971).

and biochemical

i: 107-109 (1988).

&

M.H.

Reactivation complexes.

of

FEBS

metal

Letters.

& Suszkiw, J.B. Permeation of Pb +2 through calcium channels:

in

K.

isolated

&

of

bovine

Maneesha,

Biol.

voltage

and

dihydropitidine

chromaffin

cells.

Effect

Pb +2

Biophys

Acta

Biochem.

of

lead

on

nitrogenase

in a cyanobacterium Nostoc

29:116-119

and glutathione

enzyme

muscorum.

of

Indian

J.

P. Phytochelatin synthesis

levels under cadmium stress

(l.f.)

and

~1991).

Tripathi, R.D., Rai, U.N., Gupta, M. & Chandra, verticillata

sensitive

(1991).

nitrogen assimilation Exp.

E.L.

lead

Sci.

by phytochelatin metal

measurements

1069:197-200 Trehan,

of

(1991).

Tomsing, J,L. entry

zinc.

41:91-108

Biol.

distribution

effect of lead on higher plants. Vegetas° Thuman,

&

orthophosphate

transpiratin stream of higher plants. Pest. Thapa,

inhibition

(1985).

C.J. T.W.

the

Differential tolerance of

microscope and diffraction studies. J. Cell. Tandon,

and

{1976).

T. & Bradshaw, to

capillaris

i01:309-316

of

19:1-6

Royle.

Bull.

Env.

Mehra,

R.K.

in aquatic weed hydrilla

Contam.

56:

Toxicol

505-512

(1996). Tripathi,

R.D.,

Yunus,

metallthioneins in plants 2 : 1 - 4 UNEP/WHO.

Lead

M.

&

C.

and

Phyto-

(1996).

(Environmental

Health

Criteria

Proforma/World Health Organization, Urquhart,

Phytochelatins

: Potential of these unique metal detoxifying systems

Genetics

of

lead

3) Geneva

UN

Environmental

21-27 (1977).

tolerance

in Fesluca

ovina.

26:

Heredity.

19-33 (1971). Van

Assche,

F.

&

Clijsters,

H.

Effect

plants. Plant cell and Environment. Venkataraman,

S., Veeranianeyulu,

of

metals

13:195-206

lime

A.,

Muller,

and

beans. Agron. Wallace,

A.,

effect

R.T.,

chelating

high

S.m., levels

bush bean. Co~mun.

J.W. on

J. 6 6 : 6 9 8 - 7 0 0

Soufi, of

Cha,

agent

16:615-616

& Alexander,

micronutrients

activity

in

G.V. in

(1978). Soil

soybeans

pH,

excess

and

bush

(1974).

Alexander, of

enzyme

(1971).

K. & Ramdas, V.S. heavy metal inhibition

of nitrate reductase. Ind. J. Exp. Biol. Wallace,

on

DTPA

C.V. and

Soil Plant Annal.

& Cha,

EDDHA

on

7:111-116

J.W.

Comparison

microelement (1976).

of the

uptake

in

2493 Welsh,

R.P.H.

metals

Studies

and

on uptake,

phosphorus

in

translocation aquatic

and accumulation

plants.

Ph.D.

Thesis,

of trace Westfield

College, University of London, pp. 331 (1977). Wheeler,

G.L.

and

the

& Rolfe, G.L. The relationship between daily traffic volume distribution

Environ. Pollut.

of

lead

in

roadside

soil

and

vegetation.

265-274 (1976).

Wierzbicka, M. lead accumulation and its translocation barrier in roots of AlliuJ

cepa

L.

autoradiographic

Cell Environment i 0 : 1 7 - 2 6 Wu,

L.

& Antonovics,

Lead

tolerance

and

J. Experimental in Plantago

ecological

lanceolata

roadside. Ecology. 5 7 : 2 0 5 - 2 0 8 Zhou, J., Goldsbrough,

ultrastructural

and

or

R.L. lime

genetics Cynodon

in Plantago dactylon

II.

from

a

P.B. Formational homologs of fungal metallothionein

& Faster, J.M. or

Plant

(1976).

genes from Arabidopsis, Plant Cell 6 : 8 7 5 - 8 8 4 Zimdahl,

studies.

(1987).

uptake

of

(1994).

The influence of applied phosphorus, lead

from

soil.

J.

Environ.

Qual.

5:

manure 31-34

(1976). Zimdahl, R.L. & Koeppe, D.E. Uptake by plants. (eds.

Boggerss,

W.R.

&

Wixon,

B.B.).

Washington, DC., USA, pp. 99-104 (1977).

In: lead in the Environment

National

Science

Foundation,