Handbook of Plant Nutrition - chapter 10 pdf

10
Copper
David E. Kopsell
University of Wisconsin-Platteville, Platteville, Wisconsin
Dean A. Kopsell
University of Tennessee, Knoxville, Tennessee
CONTENTS
10.1 The Element Copper 293
10.1.1 Introduction 293
10.1.2 Copper Chemistry 294
10.2 Copper in Plants 294
10.2.1 Introduction 294
10.2.2 Uptake and Metabolism 294
10.2.3 Phytoremediation 313
10.3 Copper Deficiency in Plants 314
10.4 Copper Toxicity in Plants 315
10.5 Copper in the Soil 316
10.5.1 Introduction 316
10.5.2 Geological Distribution of Copper in Soils 317
10.5.3 Copper Availability in Soils 317
10.6 Copper in Human and Animal Nutrition 321
10.6.1 Introduction 321
10.6.2 Dietary Sources of Copper 321
10.6.3 Metabolism of Copper Forms 321
10.7 Copper and Human Health 322
10.7.1 Introduction 322
10.7.2 Copper Deficiency and Toxicity in Humans 322
References 323
10.1 THE ELEMENT COPPER
10.1.1 I
NTRODUCTION

Copper is one of the oldest known metals and is the 25th most abundant element in the Earth’s crust.
The words ‘aes Cyprium’ appeared in Roman writings describing copper, to denote that much of
the metal at the time came from Cyprus. Refinement of copper metal dates back to 5000 BC. The
metal by itself is soft, but when mixed with zinc produces brass and when mixed with tin produces
bronze. Copper is malleable, ductile, and a good conductor of electricity. In its natural state, it is a
reddish solid with a bright metallic luster.
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10.1.2 COPPER CHEMISTRY
Copper has an atomic number 29 and atomic mass of 63.55. It belongs to Group I-B transition met-
als. The melting point of copper is 1084.6°C. Copper occurs naturally in the cuprous (I, Cu
ϩ
) and
cupric (II, Cu
2ϩ
) valence states. There is a single electron in the outer 4s orbital. The 3d
10
orbital
does not effectively shield this outer electron from the positive nuclear charge, and therefore the 4s
1
electron is difficult to remove from the Cu atom (1). The first ionization potential is 7.72 eV and the
second is 20.29 eV. Because the second ionization potential is much higher than the first, a variety
of stable Cu
ϩ
species exist (2). The ionization state of copper depends on the physical environment,
the solvent, and the concentration of ligands present. In solution, copper is present as Cu
2ϩ
or com-
plexes of this ion. The cuprous ion Cu
1ϩ

is unstable in aqueous solutions at concentrations greater
than 10
Ϫ7
M (3). However, in wet soils, Cu
1ϩ
is moderately stable at typically expected conditions
(10
Ϫ6
to 10
Ϫ7
M). Under such conditions, hydrated Cu
1ϩ
would be the dominant copper species (1).
Copper can exist as two natural isotopes,
63
Cu and
65
Cu, with relative abundances of 69.09 and
30.91%, respectively (4). In the Earth’s crust, copper is present as stable sulfides in minerals rather
than silicates or oxides (3). The Cu
1ϩ
ion is present more commonly in minerals formed at consid-
erable depth, whereas Cu
2ϩ
is present close to the Earth’s surface (3).
The transition metals are noted for the variety of complexes they form with bases. In these com-
plexes, Cu
1ϩ
and Cu
2ϩ

act as electron acceptors. Chelating bases are so named because they have
two or more electron donor sites (often on O, S, or N atoms) that form a ‘claw’ around the copper
ion (1). Such complexes are important in soil chemistry and in plant nutrition. The Cu
1ϩ
ion forms
strong complexes with bases containing S, but Cu
2ϩ
does not. In the presence of these bases, Cu
2ϩ
acts as a strong oxidant (2).
10.2 COPPER IN PLANTS
10.2.1 I
NTRODUCTION
Copper was identified as a plant nutrient in the 1930s (5,6). Prior to this realization, one of the first
uses of copper in agriculture was in chemical weed control (7). Despite its essentiality, copper is
toxic to plants at high concentrations (8). Uptake of copper by plants is affected by many factors
including the soil pH, the prevailing chemical species, and the concentration of copper present in
the soil. Once inside the plant, copper is sparingly immobile. Accumulation and expression of toxic
symptoms are often observed with root tissues. Extensive use of copper-containing fungicides in
localized areas and contamination of soils adjacent to mining operations has created problems of
toxicity in some agricultural regions. Because of this problem, remediation of copper and
identification of tolerant plant species are receiving increased attention. Concentrations of copper
in some plant species under different cultural conditions are reported in Table 10.1.
10.2.2 UPTAKE AND METABOLISM
The rate of copper uptake in plants is among the lowest of all the essential elements (9). Uptake of
copper by plant roots is an active process, affected mainly by the copper species. Copper is most
readily available at or below pH 6.0 (4). Most sources report copper availability in soils to decrease
above pH 7.0. Increasing soil pH will cause copper to bind more strongly to soil components.
Copper bioavailability is increased under slightly acidic conditions due to the increase of Cu
2ϩ

ions
in the soil solution. On two soils in Spain, with similar pH values (8.0 and 8.1) but with different
copper levels (0.64 and 1.92 mg Cu kg
Ϫ1
, respectively), leaf content of willow leaf foxglove
(Digitalis obscura L.) was equal, i.e., 7mg kg
Ϫ1
dry weight on both soils (10). Copper concentra-
tions of tomato (Lycopersicon esculentum Mill.) and oilseed rape (canola, Brassica napus L.)
roots and shoots were significantly higher in an acidic soil (pH 4.3) than in a calcareous soil (pH
8.7) (11). In contrast, however, if a mixture of Cd (II), Cu (II), Ni(II), and Zn(II) was applied to
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Copper 295
TABLE 10.1
Copper Tissue Analysis Values of Various Plant and Crop Species
Copper Concentration in Dry Matter
Plant
(mg kg
ϪϪ
1
Unless Otherwise Noted)
b
Common and
Type of Type of Tissue Age, Stage, Condition,
Scientific Name Variety Culture
a
Sampled or Date of Sample Cu Treatment
Low Medium High Reference
Alfalfa

Mesa Greenhouse soil Shoot
15 days after
20 mg kg
Ϫ1
, pH 4.5
∼85
12
(Medicago sativa
L.)
planting
20 mg kg
Ϫ1
, pH 5.8
~70
25 mg kg
Ϫ1
, pH 7.1
∼115
Artemesia, wormwood
Native soil Leaves
1.03 Ϯ
0.48 mg kg
Ϫ1
0.1
21.6 64.0 37
(Artemisia absinthium
L.)
Flowers Mature
0.1
23.3 69.4

Roots
0.1
14.3 48.9
Artemesia, white sage
Native soil Leaves
1.68 Ϯ1.04 mg kg
Ϫ1
0.1
18.5 66.9
(Artemisia ludoviciana
Flowers Mature
0.1
24.7 108.3
Nutt.)
Roots
0.1
12.6 49.6
Bean
IAPAR 57 Greenhouse Total plant 30 days old
0 mmol kg
Ϫ1
7.5
77
(Phaseolus vulgaris
L.)
soil culture
0.1 mmol kg
Ϫ1
7.5
0.2 mmol kg

Ϫ1
7.5
0.5 mmol kg
Ϫ1
10
1.0 mmol kg
Ϫ1
21.5
2.0 mmol kg
Ϫ1
38
0 mmol kg
Ϫ1
, 1.0
7
chicken manure
0.1 mmol kg
Ϫ1
, 1.0
9
chicken manure
0.2 mmol kg
Ϫ1
, 1.0
9.5
chicken manure
0.5 mmol kg
Ϫ1
, 1.0
10

chicken manure
1.0 mmol kg
Ϫ1
, 1.0
13
chicken manure
2.0 mmol kg
Ϫ1
, 1.0
17
chicken manure
Continued
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296 Handbook of Plant Nutrition
TABLE 10.1 (
Continued
)
Copper Concentration in Dry Matter
Plant
(mg kg
ϪϪ
1
Unless Otherwise Noted)
b
Common and
Type of Type of Tissue Age, Stage, Condition,
Scientific Name Variety Culture
a
Sampled or Date of Sample Cu Treatment
Low Medium High Reference

Dwarf Native soil Edible portion Mature
18
Ϯ 1mg kg
Ϫ1
,
6.6
38
bean
pH 6.1, 1.9%
modus
organic matter
326 Ϯ15 mg kg
Ϫ1
,
6.7
pH 7.0, 3.4%
organic matter
430 Ϯ20 mg kg
Ϫ1
,
7.3
pH 6.1, 2.3%
organic matter
Beet, Sugar
Native soil Roots
Mature
90 mg kg
Ϫ1
52
9

(Beta vulgaris
L.)
125 mg kg
Ϫ1
2.5
210 mg kg
Ϫ1
3.5
Carrot
Rotin and Native soil Root
Mature
18
Ϯ 1mg kg
Ϫ1
,
5.1
38
(Daucus carota
L.) sperlings
pH 6.1, 1.9%
organic matter
326 Ϯ15 mg kg
Ϫ1
,
8.1
pH 7.0, 3.4%
organic matter
430 Ϯ20 mg kg
Ϫ1
,

7.2
pH 6.1, 2.3%
organic matter
Celery
Native soil Tuber
Mature
18 Ϯ1 mg kg
Ϫ1
,
7.5
8
(Apium graveolens
var.
pH 6.1, 1.9%
dulce Pers.)
organic matter
326 Ϯ15 mg kg
Ϫ1
,1
2
pH 7.0, 3.4%
organic matter
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Copper 297
430 Ϯ
20 mg kg
Ϫ1
,1
3
pH 6.1, 2.3%

organic matter
Chickpea
Tyson Soil pot culture Shoots 62 days old,
0.06 mg kg
Ϫ1
2.5 µg pot
Ϫ1
33
(Cicer arietinum
L.)
5 plant per pot
DTPA-extractable
ϩ
0 µg pot
Ϫ1
, pH 6.4
0.06 mg kg
Ϫ1
3.8 µg pot
Ϫ1
DTPA-extractable
ϩ
100 µg pot
Ϫ1
, pH 6.4
0.06 mg kg
Ϫ1
5.5 µg pot
Ϫ1
DTPA-extractable

ϩ
200 µg pot
Ϫ1
, pH 6.4
0.06 mg kg
Ϫ1
8.0 µg pot
Ϫ1
DTPA-extractable
ϩ
400 µg pot
Ϫ1
, pH 6.4
0.06 mg kg
Ϫ1
11.3 µg pot
Ϫ1
DTPA-extractable
ϩ
800 µg pot
Ϫ1
, pH 6.4
Chinese cabbage Nagaoka Native soil Lea
ves 35 days
16 mg kg
Ϫ1
, 5 mg
21
119
(Brassica pekinensis

50
50 days
kg
Ϫ1
DTPA-extractable,
17
Rupr.)
65 days
calcareous soil, pH 8.6
15
80 days
12
90 days
11
Xiayangbai Nutrient Shoots
Full strength Hoagland
18.4
22
solution culture
solution ϩ0 mg Cu L
Ϫ1
Full strength Hoagland
40.1
solution
ϩ 0.5mg Cu L
Ϫ1
Full strength Hoagland
36.8
15 days old
solution

ϩ 1mg Cu L
Ϫ1
Full strength Hoagland
200.0
solution
ϩ 4mg Cu L
Ϫ1
Roots
Full strength Hoagland
160.3
solution ϩ0 mg Cu L
Ϫ1
Full strength Hoagland
278.8
solution
ϩ 0.5mg Cu L
Ϫ1
Continued
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TABLE 10.1 (
Continued
)
Copper Concentration in Dry Matter
Plant
(mg kg
ϪϪ
1
Unless Otherwise Noted)
b
Common and

Type of Type of Tissue Age, Stage, Condition,
Scientific Name Variety Culture
a
Sampled or Date of Sample Cu Treatment
Low Medium High Reference
Full strength Hoagland
349.7
solution
ϩ 1mg Cu L
Ϫ1
Full strength Hoagland
2436.0
solution
ϩ 4mg Cu L
Ϫ1
Corn (Zea mays
L.)
Native soil Seeds
Mature
90 mg kg
Ϫ1
22
9
125 mg kg
Ϫ1
1.5
210 mg kg
Ϫ1
2.5
Native soil Grain

Mature
25.89
Ϯ 2.78mg kg
Ϫ1
4.13
15
37.19
Ϯ 17.41mg kg
Ϫ1
3.60
54.39
Ϯ 8.70mg kg
Ϫ1
4.53
181.68
Ϯ 49.12mg kg
Ϫ1
3.60
Stem
Mature
25.89
Ϯ 2.78mg kg
Ϫ1
5.40
37.19
Ϯ 17.41mg kg
Ϫ1
6.61
54.39
Ϯ 8.70mg kg

Ϫ1
10.14
181.68
Ϯ 49.12mg kg
Ϫ1
24.09
Roots
Mature
25.89
Ϯ 2.78mg kg
Ϫ1
16.74
37.19
Ϯ 17.41mg kg
Ϫ1
22.28
54.39
Ϯ 8.70mg kg
Ϫ1
25.37
181.68
Ϯ 49.12mg kg
Ϫ1
108.89
Cucumber
Vert long Sand/ solution Leaves Expanding
0.5 µM CuCl
2
·H
2

O11
14
(Cucumis sativus
L.) mariacher culture
Mature
0.5 µM CuCl
2
·H
2
O14
23 34
Expanding
10 µg g
Ϫ1
substrate 27
35
ϩ 0.5
µM CuCl
2
·H
2
O
Mature
10 µg g
Ϫ1
substrate 23
25
ϩ 0.5
µM CuCl
2

·H
2
O
Bermudagrass
Native soil Shoot
Mature
2.55 Ϯ0.56 mg kg
Ϫ1
,
14.81
59
(Cynodon dactylon
1.10
Ϯ 0.09mg kg
Ϫ1
Steud.)
DTPA-extractable,
pH 5.32
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198 Ϯ
22 mg kg
Ϫ1
,
22.26
6.95 Ϯ2.15 mg kg
Ϫ1
DTPA-extractable,
pH 6.13
Roots

2.55 Ϯ
0.56 mg kg
Ϫ1
,
20.75
1.10
Ϯ 0.09mg kg
Ϫ1
DTPA-extractable,
pH 5.32
198 Ϯ
22 mg kg
Ϫ1
,
45.56
6.95 Ϯ2.15 mg kg
Ϫ1
DTPA-extractable,
pH 6.13
Willow-leaf foxglove Wild Native soil Lea
ves
0.87 mg kg
Ϫ1
10
10
(Digitalis obscura
L.) population
0.84 mg kg
Ϫ1
8

0.64 mg kg
Ϫ1
7
1.92 mg kg
Ϫ1
7
Shiny elsholtzia
Nutrient Shoots Mature
500
µM
1133
55
(Elsholtzia splendens
solution
1000
µM
3417
Nakai)
culture
Roots
0.12
µM3
8
1000
µM
12,752
Leaves
0.12
µM7
0

1000
µM
525
Faba bean
Fiord Soil pot culture Shoots 62 days old,
0.06 mg kg
Ϫ1
…
16
µg pot
Ϫ1
…
33
(Vicia faba
L.)
5 plant per pot
DTPA-extractable
ϩ
0 µg pot
Ϫ1
, pH 6.4
0.06 mg kg
Ϫ1
…
23
µg pot
Ϫ1
…
DTPA-extractable
ϩ

100 µg pot
Ϫ1
, pH 6.4
0.06 mg kg
Ϫ1
…
34
µg pot
Ϫ1
…
DTPA-extractable
ϩ
200 µg pot
Ϫ1
, pH 6.4
0.06 mg kg
Ϫ1
…
38
µg pot
Ϫ1
…
DTPA-extractable
ϩ
400 µg pot
Ϫ1
, pH 6.4
Continued
Copper 299
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TABLE 10.1 (
Continued
)
Copper Concentration in Dry Matter
Plant
(mg kg
ϪϪ
1
Unless Otherwise Noted)
b
Common and
Type of Type of Tissue Age, Stage, Condition,
Scientific Name Variety Culture
a
Sampled or Date of Sample Cu Treatment
Low Medium High Reference
0.06 mg kg
Ϫ1
…
50
µg pot
Ϫ1
…
DTPA-extractable
ϩ
800 µg pot
Ϫ1
, pH 6.4
Grape (Vitis vinifera
L.) Merlot, Native soil Leaves

Mature
75.1 mg kg
Ϫ1
,
276
110
3309
DTPA-extractable
Couderc
61.8 mg kg
Ϫ1
,
264
root stock
DTPA-extractable
63.0 mg kg
Ϫ1
,
279
DTPA-extractable
Musts
Mature
75.1 mg kg
Ϫ1
,
4.74 mg L
Ϫ1
DTPA-extractable
61.8 mg kg
Ϫ1

,
4.65 mg L
Ϫ1
DTPA-extractable
63.0 mg kg
Ϫ1
,
5.08 mg L
Ϫ1
DTPA-extractable
Wine
75.1 mg kg
Ϫ1
,
0.076 mg L
Ϫ1
DTPA-extractable
61.8 mg kg
Ϫ1
,
0.070 mg L
Ϫ1
DTPA-extractable
63.0 mg kg
Ϫ1
,
0.073 mg L
Ϫ1
DTPA-extractable
Kohlrabi

Native soil Edible portion Mature
18 Ϯ1 mg kg
Ϫ1
,
1.9
38
(Brassica oleracea
var.
pH 6.1, 1.9%
gongylodes
L.)
organic matter
326 Ϯ15 mg kg
Ϫ1
,
2.8
pH 7.0, 3.4%
organic matter
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430 Ϯ
20 mg kg
Ϫ1
,
2.5
pH 6.1, 2.3%
organic matter
Lentil
Digger Soil pot culture Shoots 62 days old,
0.06 mg kg

Ϫ1
0.6 µg pot
Ϫ1
33
(Lens culinaris
5 plants per pot DTPA-extractable
Medik)
ϩ
0 µg pot
Ϫ1
, pH 6.4
0.06 mg kg
Ϫ1
1.5 µg pot
Ϫ1
DTPA-extractable
ϩ 100
µg pot
Ϫ1
, pH 6.4
0.06 mg kg
Ϫ1
2.0 µg pot
Ϫ1
DTPA-extractable
ϩ 200
µg pot
Ϫ1
, pH 6.4
0.06 mg kg

Ϫ1
2.8 µg pot
Ϫ1
DTPA-extractable
ϩ 400
µg pot
Ϫ1
, pH 6.4
0.06 mg kg
Ϫ1
3.5 µg pot
Ϫ1
DTPA-extractable
ϩ 800
µg pot
Ϫ1
, pH 6.4
Lettuce
American Native soil Leaves Mature
18 Ϯ1 mg kg
Ϫ1
,1
13
8
(Lactuca sativa
L.) gathering
pH 6.1, 1.9%
brown
organic matter
326 Ϯ15 mg kg

Ϫ1
,4
0
pH 7.0, 3.4%
organic matter
430 Ϯ20 mg kg
Ϫ1
,2
1
pH 6.1, 2.3%
organic matter
Lucerne
Native soil Leaves Mature
90 mg kg
Ϫ1
12
29
(Alfalfa,
Medicago
125 mg kg
Ϫ1
11.5
sativa
L.)
210 mg kg
Ϫ1
15
Mangold
Native soil Edible portion Mature
18 Ϯ1 mg kg

Ϫ1
,1
13
8
(Beta vulgaris
L.
pH 6.1, 1.9%
var. macrorhiza)
organic matter
Continued
Copper 301
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TABLE 10.1 (
Continued
)
Copper Concentration in Dry Matter
Plant
(mg kg
ϪϪ
1
Unless Otherwise Noted)
b
Common and
Type of Type of Tissue Age, Stage, Condition,
Scientific Name Variety Culture
a
Sampled or Date of Sample Cu Treatment
Low Medium High Reference
326
Ϯ 15mg kg

Ϫ1
,1
8
pH 7.0, 3.4%
organic matter
430 Ϯ20 mg kg
Ϫ1
,2
3
pH 6.1, 2.3%
organic matter
Indian mustard
Native soil Leaves Mature
0 mg kg
Ϫ1
, 0 g kg
Ϫ1
Ͻ 10
106
(Brassica juncea
L.)
biosolid organic
carbon
50 mg kg
Ϫ1
, 0 g kg
Ϫ1
∼40
biosolid organic carbon
100 mg kg

Ϫ1
, 0 g kg
Ϫ1
∼50
biosolid organic carbon
200 mg kg
Ϫ1
, 0 g kg
Ϫ1
∼85
biosolid organic carbon
400 mg kg
Ϫ1
, 0 g kg
Ϫ1
∼200
biosolid organic carbon
Oat (Avena sativa
L.)
Native soil Stems
Mature
12.2 mg kg
Ϫ1
3.9
16
Leaves
12.2 mg kg
Ϫ1
5.5
Flowers

12.2 mg kg
Ϫ1
7.9
Roots
12.2 mg kg
Ϫ1
11.5
Native soil Tillers
Mature
3.1 mg kg
Ϫ1
,
3.9
50
DTPA-extractable
3.5 mg kg
Ϫ1
,
4.5
DTPA-extractable
2.5 mg kg
Ϫ1
,
6.1
DTPA-extractable
3.3 mg kg
Ϫ1
,
4.0
DTPA-extractable

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Onion (Allium cepa
L.)
Native soil Bulb
Mature
Ͻ 400mg kg
Ϫ1
7.1
36
Stem
Mature
Ͻ 400mg kg
Ϫ1
6.4
Leaves Mature
Ͻ 400mg kg
Ϫ1
6.6
Bulb
Mature
Ͼ 400mg kg
Ϫ1
8.2
Stem
Mature
Ͼ 400mg kg
Ϫ1
10.2
Leaves Mature

Ͼ 400mg kg
Ϫ1
10.9
Oregano (Origanum
Native soil Upper leaves Mature
12–26 µM g
Ϫ1
2.5 µmol g
Ϫ1
4.1 µmol g
Ϫ1
vulgare
L. subsp.
Lower leaves
3.5
µmol g
Ϫ1
5.5 µmol g
Ϫ1
hirtum
Soó)
Knotgrass
Native soil Shoots Mature
2.55
Ϯ 0.56mg kg
Ϫ1
,
13.35
59
(Paspalum disticum

L.)
1.10
Ϯ 0.09mg kg
Ϫ1
DTPA-extractable,
pH 5.32
99 Ϯ6.42 mg kg
Ϫ1
,
32.27
10 Ϯ2.61 mg kg
Ϫ1
DTPA-extractable,
pH 7.25
191 Ϯ
33 mg kg
Ϫ1
,
8.79
7.38 Ϯ3.2 mg kg
Ϫ1
DTPA-extractable,
pH 7.38
Roots
2.55 Ϯ
0.56 mg kg
Ϫ1
,
20.30
1.10

Ϯ 0.09mg kg
Ϫ1
DTPA-extractable,
pH 5.32
99 Ϯ6.42 mg kg
Ϫ1
,
21.48
10 Ϯ2.61 mg kg
Ϫ1
DTPA-extractable,
pH 7.25
191 Ϯ
33 mg kg
Ϫ1
,
21.38
7.38 Ϯ3.2 mg kg
Ϫ1
DTPA-extractable,
pH 7.38
Continued
Copper 303
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TABLE 10.1 (
Continued
)
Copper Concentration in Dry Matter
Plant
(mg kg

ϪϪ
1
Unless Otherwise Noted)
b
Common and
Type of Type of Tissue Age, Stage, Condition,
Scientific Name Variety Culture
a
Sampled or Date of Sample Cu Treatment
Low Medium High Reference
Pea (Pisum sativum
L.) Fenomen Solution culture Roots
21 days old
6.42
µmol cumulative
12 µg g
Ϫ1
24
treatment
fresh weight
Radish
Rimbo Solution culture Above- 28 days old
0.12
µM4
µg plant
Ϫ1
18
(Raphanus sativus
L.)
ground part

5
µM8
µg plant
Ϫ1
10 µM1
3
µg plant
Ϫ1
15 µM1
4
µg plant
Ϫ1
Below-
0.12 µM
2.3 µg plant
Ϫ1
ground part
5 µM
2.8 µg plant
Ϫ1
10 µM
3.7
µg plant
Ϫ1
15 µM
3.7
µg plant
Ϫ1
Native soil Above- 28 days old
591 Ϯ

25 mg kg
Ϫ1
,
7.0 µg plant
Ϫ1
ground part
200 Ϯ8 mg kg
Ϫ1
EDTA-
extractable, pH 6.3, 6.9%
organic matter
Red cover
Native soil Stems
Mature
12.2 mg kg
Ϫ1
8.6
16
(Trifolium pratense
L.)
Leaves
16.1
Flowers
20.2
Roots
24.2
Rhodegrass
Kallide Native soil Tillers
Mature
3.1 mg kg

Ϫ1
,
8.5
50
(Chloris gayana
Kunth)
DTPA-extractable
3.5 mg kg
Ϫ1
,
7.2
DTPA-extractable
2.5 mg kg
Ϫ1
,
10.1
DTPA-extractable
3.3 mg kg
Ϫ1
,
10.0
DTPA-extractable
Rice (Oryza sativa
L.)
Native soil Shoot
Mature
23 mg kg
Ϫ1
, pH 6.2
12

117
90 mg kg
Ϫ1
, pH 6.2
28
158 mg kg
Ϫ1
, pH 7.0
37
304 Handbook of Plant Nutrition
CRC_DK2972_Ch010.qxd 7/14/2006 12:13 PM Page 304
Rye (Secale cereale
L.)
Native soil Stems
Mature
12.2 mg kg
Ϫ1
6.9
16
Leaves
5.2
Flowers
9.0
Roots
21.9
Ryegrass
Native soil Stems
Mature
12.2 mg kg
Ϫ1

2.5
16
(Lolium multiflorum
Leaves
4.5
Lam.)
Flowers
7.5
Roots
10.9
Willow
Greenhouse Leaves 75 days old
20.22 mg kg
Ϫ1
2.54
45
(Salix acmophylla
soil pot culture
20.22 mg kg
Ϫ1
10.8
Boiss.)
ϩ 500mg kg
Ϫ1
20.22 mg kg
Ϫ1
17.2
ϩ 1000mg kg
Ϫ1
20.22 mg kg

Ϫ1
49.4
ϩ 2000mg kg
Ϫ1
20.22 mg kg
Ϫ1
82.3
ϩ 5000mg kg
Ϫ1
20.22 mg kg
Ϫ1
126.3
ϩ 10,000mg kg
Ϫ1
Stems
20.22 mg kg
Ϫ1
4.0
20.22 mg kg
Ϫ1
25.3
ϩ 500mg kg
Ϫ1
20.22 mg kg
Ϫ1
73.3
ϩ 1000mg kg
Ϫ1
20.22 mg kg
Ϫ1

103.9
ϩ 2000mg kg
Ϫ1
20.22 mg kg
Ϫ1
179.2
ϩ 5000mg kg
Ϫ1
20.22 mg kg
Ϫ1
203.7
ϩ 10,000mg kg
Ϫ1
Roots
20.22 mg kg
Ϫ1
6.85
20.22 mg kg
Ϫ1
24.8
ϩ 500mg kg
Ϫ1
Continued
Copper 305
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TABLE 10.1 (
Continued
)
Copper Concentration in Dry Matter
Plant

(mg kg
ϪϪ
1
Unless Otherwise Noted)
b
Common and
Type of Type of Tissue Age, Stage, Condition,
Scientific Name Variety Culture
a
Sampled or Date of Sample Cu Treatment
Low Medium High Reference
20.22 mg kg
Ϫ1
75.8
ϩ 1000mg kg
Ϫ1
20.22 mg kg
Ϫ1
177.5
ϩ 2000mg kg
Ϫ1
20.22 mg kg
Ϫ1
345.3
ϩ 5000mg kg
Ϫ1
20.22 mg kg
Ϫ1
624.4
ϩ 10,000mg kg

Ϫ1
Setaria, Forage Kazungula Native soil
Tillers
Mature
3.1 mg kg
Ϫ1
,
8.5
50
(Setaria sphacelata
DTPA-extractable
Moss.)
3.5 mg kg
Ϫ1
,
5.1
DTPA-extractable
2.5 mg kg
Ϫ1
,
10.4
DTPA-extractable
3.3 mg kg
Ϫ1
,
10.4
DTPA-extractable
Soybean
Williams Native soil Main stem R5
N/A

9
35
(Glycine max
Merr.) 82 and
leaves
Pioneer
Branch stem
9391
leaves
11
Main stem Mature
14
seeds
Branch stem
20
seeds
Spinach
Wonderful Nutrient Leaves Mature
0.5 µM Cu
25
73
(Spinacia oleracea
L.)
solution
160 µM Cu
729
160 µM Cu
462
ϩ 40 160
µM Fe

306 Handbook of Plant Nutrition
CRC_DK2972_Ch010.qxd 7/14/2006 12:13 PM Page 306
Roots
Mature
0.5 µM Cu
33
160 µM Cu
4727
160 µM Cu
3800
ϩ 40 160µM Fe
Sunflower
Nutrient Roots
6 days old
0.3 µM CuSO
4
42
128
(Helianthus annuus
L.)
solution
10
Ϫ5
M Cu
2ϩ
108
10
Ϫ4
M Cu
2ϩ

138
10
Ϫ3
M Cu
2ϩ
1070
Hypocotyl
0.3 µM CuSO
4
20
10
Ϫ5
M Cu
2ϩ
52
10
Ϫ4
M Cu
2ϩ
49
10
Ϫ3
M Cu
2ϩ
165
Cotyledon
0.3 µM CuSO
4
24
10

Ϫ5
M Cu
2ϩ
47
10
Ϫ4
M Cu
2ϩ
66
10
Ϫ3
M Cu
2ϩ
95
Tomato
Greenhouse soil Leaves 4th–5th fully e
xpanded 7.79 mg kg
Ϫ1
Ͻ 5mg kg
Ϫ1
…
1400 mg kg
Ϫ1
31
(Lycopersicon
DTPA-extractable Cu
esculentum
Mill.)
Native soil Fruit
Ripe

Ͻ
400 mg kg
Ϫ1
14.7
36
Stem
Mature
Ͻ 400mg kg
Ϫ1
19.5
Leaves Mature
Ͻ 400mg kg
Ϫ1
35.7
Fruit
Ripe
Ͼ 400mg kg
Ϫ1
15.8
Stem
Mature
Ͼ 400mg kg
Ϫ1
26.2
Leaves Mature
Ͼ 400mg kg
Ϫ1
64.4
Wheat
Native soil Stems

Mature
12.2 mg kg
Ϫ1
3.6
16
(Triticum aestivum
L.)
Leaves
6.1
Flowers
7.9
Roots
7.5
Native soil Shoot
Mature
14.5 g kg
Ϫ1
organic 6.4
12.5
21
Cu, 0.4 mg kg
Ϫ1
DTPA
extractable Cu
37.6 g kg
Ϫ1
organic 2.3
3.4
Cu, 2.0 mg kg
Ϫ1

DTPA
extractable Cu
Continued
Copper 307
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TABLE 10.1 (
Continued
)
Copper Concentration in Dry Matter
Plant
(mg kg
ϪϪ
1
Unless Otherwise Noted)
b
Common and
Type of Type of Tissue Age, Stage, Condition,
Scientific Name Variety Culture
a
Sampled or Date of Sample Cu Treatment
Low Medium High Reference
Native soil Grain
Mature
26.03
Ϯ 2.56mg kg
Ϫ1
3.47
15
34.72 Ϯ16.38mg kg
Ϫ1

6.84
87.40 Ϯ62.24 mg kg
Ϫ1
2.91
199.26 Ϯ66.54mg kg
Ϫ1
6.84
Stem
Mature
26.03 Ϯ2.56 mg kg
Ϫ1
4.62
34.72 Ϯ16.38 mg kg
Ϫ1
4.54
87.40 Ϯ62.24 mg kg
Ϫ1
5.62
199.26 Ϯ66.54 mg kg
Ϫ1
6.12
Roots
Mature
26.03 Ϯ2.56 mg kg
Ϫ1
7.34
34.72 Ϯ16.38 mg kg
Ϫ1
8.68
87.40 Ϯ62.24 mg kg

Ϫ1
15.63
199.26 Ϯ66.54 mg kg
Ϫ1
40.10
Stretton Soil pot culture Shoots 62 days old,
0.06 mg kg
Ϫ1
DTPA-
6 µg pot
Ϫ1
33
5 plants per pot extractable
ϩ 0
µg pot
Ϫ1
,
pH 6.4
0.06 mg kg
Ϫ1
DTPA-
11
µg pot
Ϫ1
extractable
ϩ 100µg pot
Ϫ1
,
pH 6.4
0.06 mg kg

Ϫ1
DTPA-
18
µg pot
Ϫ1
extractable
ϩ 200µg pot
Ϫ1
,
pH 6.4
0.06 mg kg
Ϫ1
DTPA-
22
µg pot
Ϫ1
extractable
ϩ 400µg pot
Ϫ1
,
pH 6.4
0.06 mg kg
Ϫ1
DTPA-
27
µg pot
Ϫ1
extractable
ϩ 800µg pot
Ϫ1

,
pH 6.4
Sunny Nutrient Roots
21 days old
18.02 µmol cumulative
27
Ϯ 1µg g
Ϫ1
24
solution culture
treatment
fresh weight
308 Handbook of Plant Nutrition
CRC_DK2972_Ch010.qxd 7/14/2006 12:13 PM Page 308
Wheat
Creso Nutrient solution Shoots 15-day-old seedlings,
Control—
1
/2
strength
15.1
92
(Triticum durum
Desf.)
culture
168 h after treatment Hoagland’s No. 2
1
/
2
strength Hoagland’s

15.1
No. 2 ϩ150
µM
Roots
Control—
1
/2
strength
25.9
Hoagland’s No. 2
1
/2
strength Hoagland’s
2900
No. 2 ϩ150
µM
White clover
Native soil Stems
Mature
12.2 mg kg
Ϫ1
20.2
16
(Trifolium repens
L.)
Leaves
12.0
Flowers
38.0
Roots

28.4
a’
Native soil’ denotes experiments or studies where crops were harv
ested from a
field soil or natural environment and the copper level determined from a soil sample to estimate copper
fertility.
b
Information not available. When available in references, values ha
ve been expressed as an average concentration
Ϯ standard error.
Copper 309
CRC_DK2972_Ch010.qxd 7/14/2006 12:13 PM Page 309
310 Handbook of Plant Nutrition
a montmorillonite [(Al,Mg)
2
(OH)
2
Si
4
O
10
] soil at 50 mg kg
Ϫ1
each, there were no differences in
growth of alfalfa (Medicago sativa L.) between soil pH treatments of 4.5, 5.8, and 7.1, and plants
grown at pH 7.1 accumulated the highest amount copper (12). However, if soil pH is above 7.5,
plants should be monitored for copper deficiency.
Copper has limited transport in plants; therefore, the highest concentrations are often in root tis-
sues (11,13,14,15). When corn (Zea mays L.) was grown in solution cultures at 10
Ϫ5

,10
Ϫ4
, and 10
Ϫ3
M
Cu
2ϩ
, copper content of roots was 1.5, 8, and 10-fold greater respectively, than in treatments without
copper additions, with little copper translocation to shoot tissues occurring (14). On a Savannah fine
sandy loam pasture soil in Mississippi containing 12.3 mg Cu kg
Ϫ1
, analysis of 16 different forage
species revealed that root tissues accumulated the highest copper concentrations (28.8 mg kg
Ϫ1
), fol-
lowed by flowers (18.1mg kg
Ϫ1
), leaves (15.5 mg kg
Ϫ1
), and stems (8.4 mg kg
Ϫ1
) (16). Copper most
likely enters roots in dissociated forms but is present in root tissues as a complex. Nielsen (17)
observed that copper uptake followed Michaelis–Menten kinetics, with a K
m
ϭ 0.11µmol L
Ϫ1
and a
mean C
min

ϭ 0.045µmol L
Ϫ1
over a copper concentration range of 0.08 to 3.59 µmol L
Ϫ1
. Within
roots, copper is associated principally with cell walls due to its affinity for carbonylic, carboxylic,
phenolic, and sulfydryl groups as well as by coordination bonds with N, O, and S atoms (18). At high
copper supply, significant percentages of copper can be bound to the cell wall fractions. Within green
tissues, copper is bound in plastocyanin and protein fractions. As much as 50% or more of plant copper
localized in chloroplasts is bound to plastocyanin (19). The highest concentrations of shoot
copper usually occur during phases of intense growth and high copper supply (9).
Accumulation of copper can be influenced by many competing elements (Table 10.2). Copper
uptake in lettuce (Lactuca sativa L.) in nutrient solution culture was affected by free copper ion activ-
ity, pH of the solution, and concentration of Ca
2ϩ
(20). Copper concentration of four Canadian wheat
(Triticum aestivum L.) cultivars was affected by cultivar and applied nitrogen, but the variance due to
applied nitrogen was fourfold greater than that due to cultivar (21). In Chinese cabbage (Brassica
pekinensis Rupr.), iron and phosphorus deficiencies in nutrient solution stimulated copper uptake, but
abundant phosphorus supply decreased copper accumulation (22). Fertilizing a calcareous soil (pH 8.7,
144 µg Cu g
Ϫ1
) with an iron-deficient solution increased copper accumulation by roots and shoots in
two wheat cultivars from 6 to 25µg Cu g
Ϫ1
(cv. Aroona) and 8 to 29 µg Cu g
Ϫ1
(cv. Songlen) (13). In
this same study, zinc deficiency did not significantly stimulate copper accumulation (13). Iron
deficiency in nutrient solution culture increased copper and nitrogen leaf contents uniformly along corn

leaf blades (23). Selenite (SeO
3
Ϫ2
) and selenate (SeO
4
Ϫ2
) depressed copper uptake, expressed as a per-
centage of total copper supplied, in pea (Pisum sativum L.), but not in wheat (Triticum aestivum L. cv.
Sunny). However, copper uptake and tissue concentration were not affected by selenium (24).
Iron and copper metabolism appear to be associated in plants and in yeast (25,26). Ferric-chelate
reductase is expressed on the root surface of plants and the plasma membrane of yeast under condi-
tions of iron deficiency (25). Lesuisse and Labbe (27) reported that ferric reductase reduces Cu
2ϩ
in
yeast and may be involved in copper uptake. Increases in manganese, magnesium, and potassium
accumulation were associated with iron deficiency in pea, suggesting that plasma reductases may have
a regulatory function in root ion-uptake processes via their influence on the oxidation–reduction sta-
tus of the membrane (25,26). Evidence of this process was also supported by findings in a copper-sen-
sitive mutant (cup1-1) of mouse-ear cress (Arabidopsis thaliana L. Heynh var. Columbia), suggesting
that defects in iron metabolism may influence copper accumulation in plants (25).
The copper requirements among different plant species can vary greatly, and there can also be
significant within-species variation of copper accumulation (28,29). The median copper concentration
of forage plants in the United States was reported to be 8 mg kg
Ϫ1
for legumes (range 1 to 28mg kg
Ϫ1
)
and 4 mg kg
Ϫ1
for grasses (range 1 to 16 mg kg

Ϫ1
) (30). The copper content of native pasture plants in
central southern Norway ranged from 0.9 to 27.2 mg kg
Ϫ1
(28). Copper concentrations of tomato leaves
from 105 greenhouses in Turkey ranged from 2.4 to 1490 mg kg
Ϫ1
(31). Vegetables classified as hav-
ing a low response to copper applications are asparagus (Asparagus officinalis L.), bean (Phaseolus
vulgaris L.), pea, and potato (Solanum tuberosum L.). Vegetables classified as having a high response
CRC_DK2972_Ch010.qxd 7/14/2006 12:13 PM Page 310
Copper 311
to copper are beet (Beta vulgaris L. Crassa group), lettuce, onion (Allium cepa L.), and spinach
(Spinacia oleracea L.) (32). In Australia, the critical copper concentration in young shoot tissue was
4.6 mg kg
Ϫ1
for lentil (Lens culinaris Medik), 2.8 mg kg
Ϫ1
for faba bean (Vicia faba L.), 2.6 mg kg
Ϫ1
for chickpea (Cicer arietinum L.), and 1.5 mg kg
Ϫ1
for wheat (Triticum aestivum L.) (33). Leaves of
dwarf birch (Betula nana L.) had considerably lower copper levels than mountain birch (Betula pubes-
cens Ehrh.) and willow (Salix spp.) in central southern Norway (28).
The response of many crops to copper addition depends on their growth stages (20,34). In soy-
bean (Glycine max Merr.), the copper content of branch seeds was 20 µg g
Ϫ1
whereas seeds from the
main stems contained 14 µg g

Ϫ1
(35). Addition of 10µg CuCl
2
и2H
2
O g
Ϫ1
to nutrient solution culture
significantly suppressed leaf area in expanding cucumber (Cucumis sativus L.) leaves, whereas cop-
per addition significantly limited photosynthesis in mature leaves (34). However, the suppression in
photosynthesis was attributed to an altered source–sink relationship rather than the toxic effect of
copper (34). Nitrogen and copper were the only elements that showed no gradation in concentration
along the entire corn leaf blade (23).
TABLE 10.2
Descriptions of the Interaction of Copper in Plant Tissues with Various Elements
Element Interaction with Cu in Plant Tissues
a
Nitrogen (N) Increasing levels of N fertilizers may increase requirement for Cu due to increased growth
N fertilization linearly increases the Cu content of shoots
High N levels may also inhibit translocation of Cu
Phosphorus (P) Heavy use of P fertilizers can induce Cu deficiencies in citrus
Excess P in solution culture decreased Cu accumulation in Brassica
b
Potassium (K) Foliar K sprays have reduced the copper content of pecan
Calcium (Ca) Ca was shown to reduce Cu uptake in nutrient solution culture in lettuce
c
Increasing Ca in solution culture improved reduced growth due to Cu toxicity
in mung bean
d
Iron (Fe) High levels of Fe have produced leaf chlorosis in citrus and lettuce

Fe deficiency has stimulated copper uptake in solution culture in Brassica
y
and corn
e
Excess Fe in nutrient solution culture lessened the effects of Cu toxicity in spinach
f
Zinc (Zn) Cu significantly inhibits the uptake of Zn
Zn will inhibit the uptake of Cu
Zn is believed to interfere with the Cu absorption process
Manganese (Mn) Cu has been shown to stimulate uptake of Mn in several plant species
Molybdenum (Mo) Cu interferes with the role of Mo in the enzymatic reduction of nitrate
A mutual antagonism has been found between Cu and Mo in several plant species
Aluminum (Al) Al has been shown to adversely affect the uptake of Cu
a
Reproduced from H.A. Mills, J.B. Jones, Jr., in Plant Analysis Handbook II, MicroMacro Publishing, Inc., Athens, GA,
1996, 422pp., unless otherwise noted. With permission.
b
Adapted from Z. Xiong, Y. Li, B. Xu, Ecotoxic Environ. Safety, 53:200–205, 2002.
c
Adapted from T. Cheng, H.E. Allen, Environ. Toxic Chem., 20:2544–2511, 2001.
d
Adapted from Z. Shen, F. Zhang, F. Zhang, J. Plant Nutr., 21:1153–1162, 1998.
e
Adapted from A. Mozafar, J. Plant Nutr., 20:999–1005, 1997.
f
Adapted from G. Ouzounidou, I. Illias, H. Tranopoulou, S. Karataglis, J. Plant Nutr., 21:2089–2101, 1998.
CRC_DK2972_Ch010.qxd 7/14/2006 12:13 PM Page 311
312 Handbook of Plant Nutrition
The copper content of many edible plant parts is not correlated to the amount of soil copper
(15,36,29,37,38). No correlations could be made between the level of applied copper and the

amount of that metal in edible parts of corn grain, sugar beet (Beta vulgaris L.) roots, and alfalfa
leaves (29). Despite differences of mean soil copper levels ranging from 160 to 750 mg kg
Ϫ1
, cop-
per concentrations of edible tomato fruit and onion bulbs were similar (36). Although soil copper
levels ranged from 26 to 199 mg kg
Ϫ1
, spring wheat (Triticum aestivum L.) grain accumulated only
between 2.12 and 6.84 mg Cu kg
Ϫ1
(15). Comparing a control soil containing 18 mg Cu kg
Ϫ1
and a
slag-contaminated soil containing 430 mg Cu kg
Ϫ1
, the respective copper concentrations for bean
(Phaseolus vulgaris L.) were 6.6 and 6.7 mg Cu kg
Ϫ1
dry weight; for kohlrabi (Brassica oleracea
var. gongylodes L.) were 1.9 and 2.8 mg Cu kg
Ϫ1
dry weight; for mangold (Beta vulgaris L. cv.
macrorhiza) were 11 and 18 mg Cu kg
Ϫ1
dry weight; for lettuce were 11 and 40 mg Cu kg
Ϫ1
dry
weight; for carrot (Daucus carota L.) were 5.1 and 8.1 mg Cu kg
Ϫ1
dry weight; and for celery

(Apium graveolens var. dulce Pers.) were 7.5 and 12mg Cu kg
Ϫ1
dry weight (38).
Proportionally less accumulation of cadmium, lead, and copper occurred in Artemisia species
in Manitoba, Canada, at high soil metal concentrations than in soils with low metal concentrations
(37). Radish (Raphanus sativus L.) accumulated only 5 µg Cu plant
Ϫ1
when grown on an agricul-
tural soil (pH 6.3, 6.9% organic matter) contaminated with 591mg Cu kg
Ϫ1
(18). On the other hand,
increasing copper treatments from 0.3 µM CuSO
4
to 10
Ϫ5
,10
Ϫ4
, and 10
Ϫ3
M Cu
2ϩ
increased root
copper levels in sunflower (Helianthus annuus L.) from 42, 108, 138, and 1070µg Cu g
Ϫ1
dry
weight, respectively, but not at the expense of growth (39). Contrary to results from many uptake
and accumulation studies, the above ground portions of H. annuus in this study accumulated more
copper than the roots (39).
Fertilizer sources of copper include copper chelate (Na
2

CuEDTA [13% Cu]), copper sulfate
(CuSO
4
и5H
2
O [25% Cu]), cupric oxide (CuO [75% Cu]), and cuprous oxide (Cu
2
O [89% Cu])
(Table 10.3). The copper in micronutrient fertilizers is mainly as CuSO
4
и5H
2
O and CuO (40) with
CuSO
4
и5H
2
O being the most common copper source because of its low cost and high water solubil-
ity (41). Copper can be broadcasted, banded, or applied as a foliar spray. Foliar application of
chelated copper materials can be used to correct deficiency during the growing season (41).
TABLE 10.3
Copper Fertilizer Sources and Their Approximate Copper Content
Source Chemical Formula % Cu
Cuprous oxide Cu
2
O89
Cupric oxide CuO 80
Chalcocite Cu
2
S80

Malachite, cupric carbonate CuCO
3
иCu(OH)
2
57
Copper(II) sulfate-hydroxide CuSO
4
и3Cu(OH)
2
13–53
Copper chloride CuCl
2
47
Copper frits frits 40–50
Copper(II) oxalate CuC
2
O
4
и2H
2
O40
Copper(II) sulfate monohydrate CuSO
4
иH
2
O35
Copper(II) sulfate pentahydrate CuSO
4
и5H
2

O25
Chalcopyrite CuFeS
2
35
Copper(II) ammonium phosphate Cu(NH
4
)PO
4
иH
2
O32
Copper(II) acetate Cu(C
2
H
3
O
2
)
2
иH
2
O32
Cupric nitrate Cu(NO
3
)иnH
2
O31
Copper chelates Na
2
CuEDTA 13

NaCuHEDTA 9
Organic forms Animal manures Ͻ0.5
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Copper 313
Limitations may apply to the amount of copper to be applied to land during a growing season. For
example, in Italy, additions of copper from fertilizers, including sewage sludge, cannot exceed
5 kg ha
Ϫ1
year
Ϫ1
(29). Cupric oxide was ineffective in correcting copper deficiency in the year of appli-
cation but did show residual effects in subsequent years (42). Copper sulfate has been shown to
increase the yield of plantlet regeneration from callus in tissue culture (43). In cereal crops, copper is
required for anther and pollen development, and deficiencies can lead to pollen abortion and male
sterility (44). When the concentration of copper sulfate was increased 100-fold over control treatments
to 10 µM, the rate of responding anthers in barley (Hordeum vulgare L.) increased from 57 to 72%
and the number of regenerated plantlets per responding anther increased from 2.4 to 11% (44).
10.2.3 PHYTOREMEDIATION
Heavy metal contamination of agricultural soils, aquatic waters, and ground water can pose serious
environmental and health concerns (45). Experimentation into the phyotoextraction of copper from
soils is limited (46). However, approximately 24 copper-hyperaccumulating plant species have been
reported, including members of Cyperaceae, Lamiaceae, Poaceae, and Scrophulariaceae families
(46). Reportedly, the only true copper-accumulating plants are from the central African countries of
Zaïre and Zambia (47,48). The political instability of these regions makes obtaining plant material
for research experimentation difficult and has hindered the work in this area (47,48). Work by
Morrison (49) with Zaïrian copper-tolerant plants showed mint species (Aeollanthus biformifolius
De Wild) to accumulate 3920 µg Cu g
Ϫ1
dry weight; figwort species, bluehearts, (Buchnera metal-
lorum L.) to accumulate 3520µg g

Ϫ1
dry weight; gentian species (Faroa chalcophila P. Taylor) to
accumulate 700 µg g
Ϫ1
dry weight; and mint species (Haumaniastrum robertii (Robyns) Duvign. &
Plancke) to accumulate 489 µg g
Ϫ1
dry weight (47,48). Rhodegrass (Chloris gayana Kunth.),
African bristlegrass or forage setaria (Setaria sphacelata Stapf. and C.E.Hubb), two indigenous
grass species, and oat (Avena sativa L.) were evaluated for copper soil extraction in Ethiopian veg-
etable farms irrigated with wastewater from a textile factory, water from the Kebena and Akaki
Rivers, and potable tap water. The maximum copper concentration of these plants was only
10.4 mg kg
Ϫ1
dry weight. However, soil copper levels for the experiments ranged from 2.5 to 3.5 mg
kg
Ϫ1
, and these low values may indicate low copper delivery from these irrigation sources (50).
Phytochelatins are peptides [(γ-Glu-Cys)
n
Gly] produced by plants in response to heavy metal
ion exposure (51). These compounds function to complex and detoxify metal ions (52). A variety
of metal ions such as Cu
2ϩ
,Cd
2ϩ
,Pb
2ϩ
, and Zn
2ϩ

induce phytochelatin synthesis (47,48). In addi-
tion, cations Hg
2ϩ
,Ag
ϩ
,Au
ϩ
,Bi
3ϩ
,Sb
3ϩ
,Sn
2ϩ
, and Ni
2ϩ
, and anions AsO
4
3Ϫ
and SeO
3
2Ϫ
, induce
phytochelatin biosynthesis (52). Together with phytochelatin and metallothionein (cysteine-based
proteins that transports metals) (53), internal coordination and vacuolar sequestration determine the
tolerance of plant species and cultivars to heavy metals (18). No induction of phytochelatin syn-
thesis was observed following exposure to Al
3ϩ
,Ca
2ϩ
,Co

2ϩ
,Cr
2ϩ
,Cs
ϩ
,K
ϩ
,Mg
2ϩ
,Mn
2ϩ
, MoO
4
2Ϫ
,
Na
ϩ
, or V
ϩ
(52). Copper phytochelatins have been isolated from common monkeyflower (Mimulus
guttatus Fisch. ex DC) (54). Exposure of serpentine roots (Rauwolfia serpentina Benth. ex Kurz) to
50 µM CuSO
4
in hydroponic culture resulted in arrested plant growth for 10h and rapid production
of Cu
2ϩ
-binding phytochelatins. Two days after treatment, 80% of the copper in solution was
depleted from the nutrient solution, and the intercellular phytochelatin concentration reached a con-
stant level, and normal growth resumed (52).
Some plants have shown a strong potential for hyperaccumulation of copper in their tissues. A

population of aromatic madder (Elsholtzia splendens Nakai) collected on a copper-contaminated
site in the Zhejiang providence of China demonstrated phytoremediation potential after the species
was noted to accumulate 12,752 µg Cu g
Ϫ1
dry weight in roots and 3417 µg Cu g
Ϫ1
dry weight in
shoots when cultured in nutrient solutions containing 1000 µM Cu
2ϩ
(55). Alfalfa shoots accumu-
lated as much as 12,000 mg Cu kg
Ϫ1
(56). Roots of a willow species (Salix acmophylla Boiss.), an
economically important tree which grows on the banks of water bodies, accumulated nearly 7 to
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314 Handbook of Plant Nutrition
624 µg Cu g
Ϫ1
dry weight in response to increasing copper treatments in soil from 0 to 10,000 mg
kg
Ϫ1
(45). On three soils in Zambia, the roots of a grass species (Stereochlanea cameronii Clayton)
accumulated 9 to 755 µg Cu g
Ϫ1
dry weight in response to a range from 0.2 to 203 µg Cu g
Ϫ1
in
soil (57).
Evidence suggests quantitative genetic variation in the ability to hyperaccumulate heavy metals
between- and within-plant populations (58). Populations of knotgrass (Paspalum distichum L.) and

bermudagrass (Cynodon dactylon Pers.) located around mine tailings in China contained 99 to
198 mg Cu kg
Ϫ1
. These native grass populations were more tolerant to increasing CuSO
4
concen-
trations in solution culture than similar genotypes collected from sites containing much lower lev-
els of copper in soil (2.55 mg Cu kg
Ϫ1
) (59). Legumes, Lupinus bicolor Lindl. and Lotus purshianus
Clem. & Clem., growing on a copper mine site (abandoned in 1955) in northern California showed
greater tolerance to 0.2 mg Cu L
Ϫ1
in solution culture than genotypes growing in an adjacent
meadow (60). Among ten Brassicaceae, only Indian mustard (Brassica juncea L.) and radish
showed seed germination higher than 90% after 48h exposure to copper concentrations ranging
from 25 to 200 µM (18). As noted with other heavy metals, copper actually caused a slight increase
in the degree of seed germination, possibly due to changes in osmotic potential that promote water
flow into the seeds (18).
Copper toxicity limits have been established for grass species used to restore heavy metal-
contaminated sites. Using sand culture, the lethal copper concentration for redtop (Agrostis gigan-
tea Roth.) was 360 mg Cu L
Ϫ1
, for slender wheatgrass (Elymus trachycaulus Gould ex Shiners) was
335 mg Cu L
Ϫ1
, and for basin wildrye (Leymus cinereus A. Love) was 263 mg Cu L
Ϫ1
, whereas
tufted hairgrass (Deschampsia caespitosa Beauv.) and big bluegrass (Poa secunda J. Presl)

displayed less than 50% mortality at the highest treatment level of 250 mg Cu L
Ϫ1
(61).
Success has been shown with sodium-potassium polyacrylate polymers for copper remediation
in solution and sand culture; however, the cost of application is often prohibitive. This polymer
material at 0.07% dry mass in sand culture absorbed 47, 70, and 190mg Cu g
Ϫ1
dry weight at 0.5 µM,
1µM, 0.01 M Cu (as CuSO
4
и5H
2
O) in solution, respectively (62). In this experiment, the polyacrylate
polymer increased the dry weight yield of the third and fourth cutting of perennial ryegrass (Lolium
perenne L.) after 50mg Cu kg
Ϫ1
was applied.
10.3 COPPER DEFICIENCY IN PLANTS
Deficiencies of micronutrients have increased in some crop plants due to increases in nutritional
demands from high yields, use of high analysis (N, P, K) fertilizers with low micronutrient quanti-
ties, and decreased use of animal manure applications (40). Copper deficiency symptoms appear to
be species-specific and often depend on the stage of deficiency (7). Reuther and Labanauskas (7)
give a comprehensive description of deficiency symptoms for 36 crops, and readers are encouraged
to consult this reference. In general, the terminal growing points of most plants begin to show
deficiency symptoms first, a result of immobility of copper in plants. Most plants will exhibit roset-
ting, necrotic spotting, leaf distortion, and terminal dieback (7,33). Many plants also will show a
lack of turgor and discoloration of certain tissues (7,33). Copper deficiency symptoms in lentil, faba
bean, chickpea, and wheat (Triticum aestivum L.) were chlorosis, stunted growth, twisted young
leaves and withered leaf tips, and a general wilting despite adequate water supply (33).
Copper deficiency limits the activity of many plant enzymes, including ascorbate oxidase, phe-

nolase, cytochrome oxidase, diamine oxidase, plastocyanin, and superoxide dismutase (63).
Oxidation–reduction cycling between Cu(I) and Cu(II) oxidation states is required during single
electron transfer reactions in copper-containing enzymes and proteins (64). Narrow-leaf lupins
(Lupinus angustifolius L.) exhibited suppressed superoxide dismutase, manganese-superoxide dis-
mutase, and copper/zinc-superoxide dismutase activity on a fresh weight basis under copper
deficiency 24 days after sowing (65). Copper deficiency also depresses carbon dioxide fixation,
electron transport, and thylakoid prenyl lipid synthesis relative to plants receiving full nutrition (66).
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Copper 315
In brown, red, and green algae, the most severe damage in response to Cu
2ϩ
deficiency was a
decrease in respiration, whereas oxygen production was much less affected (67).
Plants differ in their susceptibility to copper deficiency with wheat (Triticum aestivum L.), oats,
sudangrass (Sorghum sudanense Stapf.), and alfalfa being highly sensitive; and barley, corn, and
sugar beet being moderately sensitive. Copper tissues levels below 2 mg kg
Ϫ1
are generally inade-
quate for plants (9). A critical copper concentration for Canadian prairie soils for cereal crops pro-
duction was reported as 0.4 mg kg
Ϫ1
(42).
10.4 COPPER TOXICITY IN PLANTS
Prior to the identification of copper as a micronutrient, it was regarded as a plant poison (7).
Therefore, no discussion of copper toxicity can rightfully begin without mention of its use as a fun-
gicide. In 1882, botanist Pierre-Marie-Alexis Millardet developed a copper-based formulation that
saved the disease-ravaged French wine industry (68). Millardet’s observation of the prophylactic
effects against downy mildew of grapes by a copper sulfate–lime mixture led to the discovery and
development of Bordeaux mixture [CuSO
4

и5H
2
O ϩ Ca(OH)
2
]. Incidentally, this copper
sulfate–lime mixture had been sprinkled on grapevines along the roadways for decades to prevent
the stealing of grapes. The observation that Bordeaux sprays sometimes had stimulating effects on
vigor and yield led to the experimentation that eventually proved the essentiality of copper as a plant
micronutrient (7). It is likely that copper fungicides corrected many copper deficiencies before cop-
per was identified as a required element (69).
The currently accepted theory behind the mode of action of copper as a fungicide is its
nonspecific denaturation of sulfhydryl groups of proteins (70). The copper ion is toxic to all plant
cells and must be used in discrete doses or relatively insoluble forms to prevent tissue damage (70).
There are a multitude of copper-based fungicides and pesticides available to agricultural producers.
Overuse or extended use of these fungicides in orchards and vineyards has produced localized soils
with excessive copper levels (71).
The two general symptoms of copper toxicity are stunted root growth and leaf chlorosis. For
ryegrass (Lolium perenne L.) seedlings in solution culture, the order of metal toxicity affecting root
growth was Cu ϩ Niϩ MnϩPb ϩ Cd ϩ ZnϩAlϩHg ϩ Cr ϩ Fe (72). This order is supported by
earlier experiments with Triticum spp., white mustard (Sinapis alba L.), bent grass (Agrostis spp. L.),
and corn (72). Stunted roots are characterized by poor development, reduced branching, thickening,
and unusual dark coloration (7,14,72,73). Small roots and apices of large roots of spinach turned
black in response to 160 µM Cu in nutrient solution culture (73). Root growth was decreased pro-
gressively in corn when plants were exposed to 10
Ϫ5
,10
Ϫ4
,10
Ϫ3
M Cu

2ϩ
in solution culture (14).
However, due to the complexity of cell elongation in roots and influences of hormones, cell wall
biosynthesis, and cell turgor, few research studies have defined the effect of copper on root growth
(74).
Copper-induced chlorosis, oftentimes resembling iron deficiency, reportedly occurs due to Cu
ϩ
and Cu
2ϩ
ion blockage of photosynthetic electron transport (75). Chlorophyll content of spinach
leaves was decreased by 45% by treatment of 160 µM Cu in solution culture over control treatment
(73). Increasing Cu
2ϩ
exposure to cucumber cotyledon and leaf tissue extracts decreased the
amount of UV-light absorbing compounds (76). Chlorosis of bean (Phaseolus vulgaris L.) and bar-
ley was observed with copper toxicity (77,78). Energy capture efficiency and antenna size were
decreased in spinach leaves exposed to toxic levels of copper (73). Copper toxicity symptoms of
oregano (Origanum vulgare L.) leaves included thickening of the lamina and increases in number
of stomata, glandular, and nonglandular hairs, as well as decreases in chloroplast number and dis-
appearance of starch grains in chloroplasts of mesophyll cells (79). Copper ions also may be respon-
sible for accelerating lipid peroxidation in chloroplast membranes (75).
In the photosynthetic apparatus, the donor and acceptor sites of Photosystem II (PSII) are sen-
sitive to excess Cu
2ϩ
ions (80). The suggested sites of Cu
2ϩ
inhibition on the acceptor side of PSII
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316 Handbook of Plant Nutrition
are the primary quinone acceptor QA (81,82), the pheophytin–QA–Fe region (83), the non-heme

Fe (82,84), and the secondary quinone acceptor QB (85). On the donor side of PSII, a reversible
inhibition of oxidation of TyrZ (oxidation–reduction active tyrosine residue in a protein compo-
nent of PSII) has been observed by Schröder et al. (86) and Jegerschöld et al. (81). However, Cu
2ϩ
ions in equal molar concentration to the number of PSII reaction centers stimulated oxygen evo-
lution nearly twofold, suggesting that Cu
2ϩ
may be a required component of PSII (80).
Substitution for magnesium in the chlorophyll heme by copper has been observed in brown and
green alga under high or low irradiance during incubation at 10 to 30µM CuSO
4
(67). High Cu
2ϩ
tissue concentrations inhibited oxygen evolution and quenched variable fluorescence (87). Brown
and Rattigan (88) reported rapid and complete oxygen production in an aquatic macrophyte
(Elodea canadensis Michx.) in response to copper toxicity. In fact, E. canadensis has been sug-
gested to be a good biomonitor of copper levels in aquatic systems (89).
Excess heavy metals often alter membrane permeability by causing leakage of K
ϩ
and other
ions. Solution culture experiments noted that 0.15µM CuCl
2
decreased hydrolytic activity of
H
ϩ
-ATPase in vivo in cucumber roots, but stimulated H
ϩ
transport in corn roots (90). During these
experiments, Cu
2ϩ

also inhibited in vitro H
ϩ
transport through the plasmalemma in cucumber roots
but stimulated transport in corn roots (90). Copper toxicity also can produce oxidative stress in
plants. Increased accumulation of the polyamine, putrescine, was detected in mung bean (Phaseolus
aureus Roxb.) after copper was increased in solution culture (91). Fifteen-day-old wheat (Triticum
durum Desf. cv. Cresco) roots exhibited a decrease in NADPH concentrations from 108 to 1.8 nmol g
Ϫ1
,
a 23% increase in glutathione reductase activity,and a 43-fold increase in ascorbate over control
plants in response to 150 µM Cu in solution culture after a 168-h exposure (94).
In soil, copper toxicity was observed with upland rice (Oryza sativa L.) at an application of
51 mg Cu kg
Ϫ1
to the soil, common bean at 37 mg kg
Ϫ1
, corn at 48 mg kg
Ϫ1
, soybean at 15 mg kg
Ϫ1
,
and wheat (Triticum aestivum L.) at 51mg kg
Ϫ1
(93). An adequate copper application rate was
3 mg kg
Ϫ1
for upland rice, 2 mg kg
Ϫ1
for common bean, 3 mg kg
Ϫ1

for corn, and 12 mg kg
Ϫ1
for wheat.
In this study, an adequate soil test for copper was 2 mg kg
Ϫ1
for upland rice, 1.5 mg kg
Ϫ1
for common
bean, 3 mg kg
Ϫ1
for corn, 1 mg kg
Ϫ1
for soybean, and 10 mg kg
Ϫ1
for wheat, when Mehlich-1
extracting solution was used. The toxic level for the same extractor was 48 mg kg
Ϫ1
for upland rice,
35 mg kg
Ϫ1
for common bean, 45 mg kg
Ϫ1
for corn, 10 mg kg
Ϫ1
for soybean, and 52 mg kg
Ϫ1
for
wheat. Copper (Cu
2ϩ
) significantly inhibited growth of radish seedlings at 1 µM in solution culture

(94). Addition of supplemental iron to nutrient solution culture lessened the effects of artificially
induced copper toxicity in spinach (73). At 10µM, Cu in the nutrient solution decreased epicotyl
elongation and fresh weight of mung bean, but increasing the calcium concentration in the solution
to 5 µM improved growth (91). Wheat net root elongation, in relation to the original length, was
only 13% in solution culture in response to 1.75 µM Cu
2ϩ
as Cu(NO
3
)
2
, but additions of 240µM
malate with the Cu(NO
3
)
2
increased root elongation to 27%; addition of 240 µM malonate increased
root to 67%, and 240 µM citrate increased growth to 91%, indicating the potential of these organic
ligands to complex Cu
2ϩ
and to lessen its toxicity (95).
10.5 COPPER IN THE SOIL
10.5.1 I
NTRODUCTION
Copper is regarded as one of the most versatile of all agriculturally important microelements in its
ability to interact with soil mineral and organic components (96). Copper can occur as ionic and
complexed copper in soil solution, as an exchangeable cation or as a specifically absorbed ion, com-
plexed in organic matter, occluded in oxides, and in minerals (97). The type of soil copper extrac-
tion methodology greatly influences recovery (98). However, soil copper levels in soils correlate
very poorly with plant accumulation and plant tissue levels.
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Copper 317
10.5.2 GEOLOGICAL DISTRIBUTION OF COPPER IN SOILS
Copper exists mainly as Cu (I) and Cu (II), but can occur in metallic form (Cu
o
) in some ores (40).
Copper occurs in soils as sulfide minerals and less stable oxides, silicates, sulfates and carbonates
(40). The most abundant copper-containing mineral is chalcopyrite (CuFeS
2
) (3). Copper can also
be substituted isomorphously for Mn, Fe, and Mg in various minerals (97).
Copper is most abundant in mafic (rich in Mg, Ca, Na, and Fe, commonly basalt and gabbro)
rocks, with minimal concentration in carbonate rocks. Mafic rocks contain 60 to 120 mg Cu kg
Ϫ1
;
ultramafic rocks (deeper in the crust than mafic rocks) contain 10 to 40 mg kg
Ϫ1
, and acid rocks
(granites, gneisses, rhyolites, trachytes, and dacites) contain 2 to 30 mg kg
Ϫ1
. Limestones and
dolomites contain 2 to10 mg Cu kg
Ϫ1
; sandstones contain 5 to 30 mg kg
Ϫ1
; shales contain about 40 mg
kg
Ϫ1
, and argillaceous sediments have about 40 to 60mg kg
Ϫ1
(9). Examples of copper-containing

minerals include malachite (Cu
2
(OH)
2
CO
3
), azurite (Cu
3
(OH)
2
(CO
3
)
2
), cuprite (Cu
2
O), tenorite
(CuO), chalcocite (Cu
2
S), covellite (CuS), chalcopyrite (CuFeS
2
), bornite (Cu
5
FeS
4
), and silicate
chrysocolla (CuSiO
3
2H
2

O) (40). Chalcopyrite (CuFeS
2
) is a brass-yellow ore that accounts for
approximately 50% of the world copper deposits. These minerals easily release copper ions during
weathering and under acidic conditions (9). The weathering of copper deposits produces blue and
green minerals often sought by prospectors (3).
Because copper ions readily precipitate with sulfide, carbonate, and hydroxide ions, it is rather
immobile in soils, showing little variation in soil profiles (9). Copper in soil is held strongly to
organic matter, and it is common to find more copper in the topsoil horizons than in deeper zones.
Four tropical agricultural soils (Bougouni, Kangaba, Baguinèda, and Gao) in Africa contained 3 to
5 mg Cu kg
Ϫ1
despite differences in climatic zone and texture (99). Copper in these soils was asso-
ciated mostly with the organic soil fraction. The minerals governing the solubility of Cu
2ϩ
in soils
are not known (100).
The global concentration of total copper in soils ranges from 2 to 200 mg kg
Ϫ1
, with a mean
concentration of 30 mg kg
Ϫ1
(40) (Table 10.4). Kabata-Pendias and Pendias (9) reported that world-
wide copper concentrations in soils commonly range between 13 and 24 mg kg
Ϫ1
. Reviews by
Kubota (30), Adriano (4), and Kabata-Pendias and Pendias (9) present detailed descriptions of
global copper distribution. The concentration of copper in soils of the United States ranges from 1
to 40 mg Cu kg
Ϫ1

, with an average content of 9 mg kg
Ϫ1
(30). Agricultural soils in central Italy
ranged from 50 to 220 mg Cu kg
Ϫ1
(29). Agricultural soils in central Chile were grouped into two
categories: one cluster containing 162mg Cu kg
Ϫ1
and another cluster containing 751 mg kg
Ϫ1
(36).
However, much of this copper was associated with very sparingly soluble forms and was of low
bioavailability to crop plants. Fifteen agricultural soils in China ranged from 5.8 to 66.1 mg Cu kg
Ϫ1
(101). Eight soils classified as Alfisols, Inceptisols, or Vertisols in India ranged from 1.12 to 5.67mg
Cu kg
Ϫ1
(102). On the other hand, alum shale and moraine soils from alum shale parent material in
India contained 65 and 112 mg Cu kg
Ϫ1
, respectively (103). Five grassland soils in the Xilin river
watershed of Inner Mongolia ranged from 0.89 to 1.62 mg Cu kg
Ϫ1
(101). Four calcareous soils
from the Baiyin region, Gansu providence, China, ranged from 26to 199 mg Cu kg
Ϫ1
, the higher
levels resulting from irrigation with wastewater from nonferrous metal mining and smelting opera-
tions in the 1950s (15). Similar copper soil concentrations were found in mine tailings (Pb–Zn) in
Guangdong providence, China (59). The mean copper content of a Canadian soil at 3 to 6.3 km from

a metal-processing smelter was 1400 to 3700 mg kg
Ϫ1
(104).
10.5.3 COPPER AVAILABILITY IN SOILS
Parent material and formation processes govern initial copper status in soils. Atmospheric input of
copper has been shown to partly replace or even exceed biomass removal from soils. Kastanozems,
Chernozems, Ferrasols, and Fluvisols contain the highest levels of copper, whereas Podzols and
Histosols contain the lowest levels.
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