Handbook of Plant Nutrition - chapter 12 pptx

12
Manganese
Julia M. Humphries, James C.R. Stangoulis,
and Robin D. Graham
University of Adelaide, Adelaide, Australia
CONTENTS
12.1 Introduction 351
12.2 Forms of Manganese and Abundance in Soils 352
12.3 Importance to Plants and Animals 352
12.3.1 Essentiality of Manganese to Higher Plants 352
12.3.2 Function in Plants 352
12.3.3 Importance to Animals 353
12.4 Absorption and Mobility 353
12.4.1 Absorption Mechanisms 353
12.4.2 Distribution and Mobility of Manganese in Plants 353
12.5 Manganese Deficiency 354
12.5.1 Prevalence 354
12.5.2 Indicator Plants 354
12.5.3 Symptoms 354
12.5.4 Tolerance 355
12.6 Toxicity 356
12.6.1 Prevalence 356
12.6.2 Indicator Plants 356
12.6.3 Symptoms 356
12.6.4 Tolerance 357
12.7 Manganese and Diseases 357
12.8 Conclusion 365
Acknowledgments 365
References 366
12.1 INTRODUCTION
The determination of manganese (Mn) essentiality in plant growth by McHargue (1914–1922)

focused the attention of plant nutritionists on this nutrient, and led the way for further ground-
breaking studies. Since then, research into the concentrations of manganese that confer deficiency
or toxicity, and the variation between- and within-plant species in their tolerance or susceptibility
to these afflictions has proliferated. The symptoms of toxicity and deficiency have also received
much attention owing to their variation among species and their similarity to other nutrient anom-
alies. The diversity of visual symptoms within a species that often confounds diagnosis has been
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attributed to soil conditions. Soil pH is one of the most influential factors affecting the absorption
of manganese by changing mobility from bulk soil to root surface. In addition to research on man-
ganese diagnostics, workers have also focused on the role of manganese in resistance to pests and
disease, revealing economically important interactions that further highlight the importance of this
nutrient in optimal plant production.
This chapter reviews literature dealing with the identification of manganese deficiency and tox-
icity in various crops of economic importance, the physiology of manganese uptake and transport,
and the interaction between manganese and diseases. In addition, a large table outlining deficient,
adequate, and toxic concentrations for various crops is included.
12.2 FORMS OF MANGANESE AND ABUNDANCE IN SOILS
Manganese is the tenth-most abundant element on the surface of the earth. This metal does not
occur naturally in isolation, but is found in combination with other elements to give many common
minerals. The principal ore is pyrolusite (MnO
2
), but lower oxides (Mn
2
O
3
,Mn
3
O
4

) and the car-
bonate are also known.
Manganese is most abundant in soils developed from rocks rich in iron owing to its association
with this element (1). It exists in soil solution as either the exchangeable ion Mn
2ϩ
or Mn
3ϩ
. Organic
chelates derived from microbial activity, degradation of soil organic matter, plant residues, and root
exudates can form metal complexes with micronutrient cations, and thereby increase manganese
cation solubility and mobility (2). Availability of manganese for plant uptake is affected by soil pH;
it decreases as the pH increases. Divalent manganese is the form of manganese absorbed at the root
surface cell membrane. As soil pH decreases, the proportion of exchangeable Mn
2ϩ
increases dra-
matically (3), and the proportions of manganese oxides and manganese bound to iron and manganese
oxides decrease (4). This action has been attributed to the increase in protons in the soil solution (5).
Acidification may also inhibit microbial oxidation that is responsible for immobilization of man-
ganese. Manganese-oxidizing microbes are the most effective biological system oxidizing Mn
2ϩ
in
neutral and slightly alkaline soils (6–8). Relatively, as soil pH increases, chemical immobilization of
Mn
2ϩ
increases (9), and chemical auto-oxidation predominates at pH above 8.5 to 9.0 (10,11).
12.3 IMPORTANCE TO PLANTS AND ANIMALS
12.3.1 E
SSENTIALITY OF MANGANESE TO HIGHER PLANTS
The first reported investigations into the essentiality of manganese by Horstmar in 1851 (12) suc-
ceeded in identifying this nutrient as needed by oats, but only where iron was in excess. Further evi-

dence for the essentiality of manganese was not made until some Japanese researchers reported that
manganese stimulated the growth of several crops substantially (13,14). These crops included rice
(Oryza sativa L.), pea (Pisum sativum L.), and cabbage (Brassica oleracea var. capitata L.), and
because of their economic importance, further interest was stimulated (15). Supporting these field
results were the physiological and biochemical studies of Bertrand (16–18). His work reported man-
ganese as having a catalytic role in plants, and that combinations with proteins were essential to
higher plant life. This reported essentiality of manganese was supported by studies by Maze (19) in
solution culture. Studies by McHargue (20,21), where the role of manganese in the promotion of
rapid photosynthesis was determined, are regarded as having established that manganese is essen-
tial for higher plant growth.
12.3.2 FUNCTION IN PLANTS
Manganese is involved in many biochemical functions, primarily acting as an activator of enzymes
such as dehydrogenases, transferases, hydroxylases, and decarboxylases involved in respiration,
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amino acid and lignin synthesis, and hormone concentrations (22,23), but in some cases it may be
replaced by other metal ions (e.g., Mg). Manganese is involved in oxidation–reduction (redox) reac-
tions within the photosynthetic electron transport system in plants (24–26). Manganese is also
involved in the photosynthetic evolution of O
2
in chloroplasts (Hill reaction). Owing to the key role
in this essential process, inhibition of photosynthesis occurs even at moderate manganese
deficiency; however, it does not affect chloroplast ultrastructure or cause chloroplast breakdown
until severe deficiency is reached (27).
12.3.3 IMPORTANCE TO ANIMALS
In humans, manganese deficiency results in skeletal abnormalities (28,29). In the offspring of man-
ganese-deficient rats, a shortening of the radius, ulna, tibia, and fibula is observed (30). Manganese
deficiency during pregnancy results in offspring with irreversible incoordination of muscles, lead-
ing to irregular and uncontrolled movements by the animal, owing to malformation of the bones
within the ear (30,31). Animals that are manganese-deficient are also prone to convulsions (32).

In contrast, manganese toxicity induces neurological disturbances that resemble Parkinson’s
disease, and the successful treatment of this disease with levodopa is associated with changes in
manganese metabolism (33,34). In animals manganese is associated with several enzymes (35),
including glycosyl transferase (36), superoxide dismutase (37,38), and pyruvate carboxylase (39).
Manganese requirement for humans is 0.035 to 0.07 mg kg
Ϫ1
, with daily intake representing 2
to 5 mg day
Ϫ1
in comparison to the body pool of 20 mg (30,40).
12.4 ABSORPTION AND MOBILITY
12.4.1 A
BSORPTION MECHANISMS
As mentioned previously, manganese is preferentially absorbed by plants as the free Mn
2ϩ
ion from
the soil solution (41–43). It readily complexes with plant and microbial organic ligands and with
synthetic chelates. However, complexes formed with synthetic chelates are generally considered to
be absorbed more slowly by roots than the free cation (44,45).
Manganese absorption by roots is characterized by a biphasic uptake. The initial and rapid
phase of uptake is reversible and nonmetabolic, with other Mn
2ϩ
and Ca
2ϩ
being exchanged freely
(46,47). In this initial phase, manganese appears to be adsorbed by the cell wall constituents of the
root-cell apoplastic space. The second phase is slower; manganese is less readily exchanged (48),
and its uptake is dependent on metabolism. Manganese is absorbed into the symplast during this
slower phase (47,48). However, the exact dependence of manganese absorption on metabolism is
not clear (46,49,50).

Uptake of manganese does not appear to be tightly controlled, unlike the major nutrient ions.
Kinetic experiments have estimated manganese absorption to be at a rate of 100 to 1000 times
greater than the need of plants (51). This may be due to the high capacity of ion carriers and chan-
nels in the transportation of manganese ions through the plasma membrane at a speed of several
hundred to several million ions per second per protein molecule (52,53).
12.4.2 DISTRIBUTION AND MOBILITY OF MANGANESE IN PLANTS
The plant part on which symptoms of Mn deficiency is observed generally indicates the mobility of the
nutrient within the plant. Manganese has been reported to be an immobile element, which is not re-
translocated (54–59), and consequently symptoms do not occur on old leaves. In addition, symptoms
of manganese deficiency regularly appear on fully expanded young leaves rather than on the newest
leaf. This symptom may indicate an internal requirement in these leaves beyond that of the new leaves
(60), or it may simply be a matter of supply and demand in what is the fastest growing tissue.
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The location of manganese in plants is a significant factor in the expression of deficiency symp-
toms and is affected by its mobility in the xylem and phloem. Manganese moves easily from the
root to the shoot in the xylem-sap transpirational stream (61). In contrast, re-translocation within
the phloem is complex, with leaf manganese being immobile, but root and stem manganese being
able to be re-mobilized (62). The net effect of the variable phloem mobility gives rise to a re-
distribution of manganese in plant parts typical of a nutrient with low phloem mobility.
Studies into the mobility of manganese with wheat (Triticum aestivum L.) (63,64), lupins
(Lupinus spp. L.) (55,65), and subterranean clover (Trifolium subterraneum L.) (56) have reported
no re-mobilization from the old leaves to the younger ones. Further support for this lack of mobil-
ity was given in a study by Nable and Loneragan (57), in which plants provided with an early sup-
ply of
54
Mn failed to re-mobilize any of this radioactive element when their roots were placed in a
solution with a low concentration of nonradioactive manganese. The apparent inconsistency with
evidence that phloem is a major source of manganese from the roots and stems to developing seeds
(59,66) can be explained by changes in carbon partitioning within the plant as Hannam and Ohki

(67) reported a re-mobilization of manganese from the stem during the outset of the reproductive
stages of plant development.
12.5 MANGANESE DEFICIENCY
12.5.1 P
REVALENCE
Manganese deficiency is most prevalent in calcareous soils, the pH of which varies from 7.3 to 8.5, and
the amounts of free calcium carbonate (CaCO
3
) also vary (68). The pH of calcareous soils is well
buffered by the neutralizing effect of calcium carbonate (69). Soils that have a high organic content, low
bulk density, and a low concentration of readily reducible manganese in the soil are also susceptible to
producing manganese deficiency. Climatically, cool and temperate conditions are most commonly asso-
ciated with manganese deficiency, although there have been reports on the same from tropical to arid
areas. Drier seasons have been reported to relieve (70) or to exacerbate (71) manganese deficiency.
12.5.2 INDICATOR PLANTS
Plants that have been reported to be sensitive to manganese deficiency are apple (Malus domestica
Borkh.), cherry (Prunus avium L.), cirtus (Citrus spp. L.), oat (Avena sativa L.), pea, beans
(Phaseolus vulgaris L.), soybeans (Glycine max Merr.), raspberry (Rubus spp. L.), and sugar beet
(Beta vulgaris L.) (72–76).
Of the cereals, oats are generally regarded as the most sensitive to manganese deficiency, with
rye (Secale cereale L.) being the least sensitive. However, there seems to be some discrepancy in
the ranking of susceptibility to manganese deficiency of wheat and barley (Hordeum vulgare L.)
(77–80). This occurrence might be attributed to a large within-species genetic variation that has
been reported for several species, including wheat (77,81), oats (78,82), barley (70,78), peas (83),
lupins (84), and soybeans (85).
Because of their sensitivity to manganese deficiency, several species previously considered sus-
ceptible to manganese deficiency have been the focus of breeding for more efficient varieties and
may therefore not be considered susceptible species in more recent publications. It is generally
agreed that grasses (Gramineae, Poaceae), clover (Trifolium spp. L.), and alfalfa (Medicago sativa L.)
are not susceptible to manganese deficiency (76,86).

12.5.3 SYMPTOMS
Characteristic foliar symptoms of manganese deficiency become unmistakable only when the
growth rate is restricted significantly (67) and include diffuse interveinal chlorosis on young
expanded leaf blades (Figure 12.1) (60); in contrast to the network of green veins seen with iron
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deficiency (67). Severe necrotic spots or streaks may also form. Symptoms often occur first on the
middle leaves, in contrast to the symptoms of magnesium deficiency, which appear on older leaves.
With eucalyptus (Eucalyptus spp. L. Her.), the tip margins of juvenile and adult expanding leaves
become pale green. Chlorosis extends between the lateral veins toward the midrib (60). With cere-
als, chlorosis develops first on the leaf base, while with dicotyledons the distal portions of the leaf
blade are affected first (67).
With citrus, dark-green bands form along the midrib and main veins, with lighter green areas
between the bands. In mild cases the symptoms appear on young leaves and disappear as the leaf
matures. Young leaves often show a network of green veins in a lighter green background, closely
resembling iron chlorosis (75). Manganese deficiency is confirmed by the presence of discoloration
(marsh spot) on pea seed cotyledons (87), and split or malformed seed of lupins (84).
In contrast to iron deficiency chlorosis, chlorosis induced by manganese deficiency is not uniformly
distributed over the entire leaf blade and tissue may become rapidly necrotic (88). The inability of man-
ganese to be re-translocated from the old leaves to the younger ones designates the youngest leaves as
the most useful for further chemical analysis to confirm manganese deficiency. Visual symptoms of
manganese deficiency can easily be mistaken for those of other nutrients such as iron, magnesium, and
sulfur (87), and vary between crops. However, they are a valuable basis for the determination of nutri-
ent imbalance (87) and, combined with chemical analysis, can lead to a correct diagnosis.
12.5.4 TOLERANCE
Tolerance to manganese deficiency is usually conferred by an ability to extract more efficiently
available manganese from soils that are considered deficient. Mechanisms that are involved in the
improved extraction of manganese from the soil include the production of root exudates (89–91),
differences in excess cation uptake thus affecting the pH of the rhizosphere (92,93), and changes in
root density (94). The genotypic variation within species for manganese efficiency can be utilized

by breeding programs to develop more efficient varieties (95,96).
Tolerance to manganese deficiency may be attributed to one or more of the following five adap-
tive mechanisms (96):
1. Superior internal utilization or lower functional requirement for manganese.
2. Improved internal re-distribution of manganese.
3. Faster specific rate of absorption from low manganese concentrations at the root–soil inter-
face.
4. Superior root geometry.
5. Greater extrusion of substances from roots into the rhizosphere to mobilize insoluble man-
ganese utilizing: (i) H
ϩ
; (ii) reductants; (iii) manganese-binding ligands; and (iv) microbial
stimulants.
Manganese 355
FIGURE 12.1 Manganese deficiency on crops: left, garden bean (Phaseolus vulgaris L.) and right, cucum-
ber (Cucumis sativus L.). (For a color presentation of this figure, see the accompanying compact disc.)
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The importance of, and evidence for, each mechanism has been reviewed extensively by
Graham (98), and so will not be re-analyzed here. It is concluded that mechanisms 1 and 2 are not
important mechanisms of efficiency generally, mechanism 3 may be important in certain situations,
while breeding for mechanism 4 is not thought to bring about rapid progress in improving tolerance.
Mechanism 5 is thought to have some role, though this area requires further investigation.
12.6 TOXICITY
12.6.1 P
REVALENCE
Manganese toxicity is a major problem worldwide and occurs mainly in poorly drained, acid soils
owing to the interactions mentioned previously. However, not all poorly drained soils are sources of
manganese toxicity as reported by Beckwith and co-workers (99), who noted that flooding often
increased the pH, thus reducing the availability of manganese. Tropical, subtropical, and temperate
soils have all been reported to be sources of manganese at concentrations high enough to produce

visible symptoms of toxicity. In the tropics, toxicity has been reported in tropical grasses grown in
the Catalina (basalt) and the Fajardo (moderately permeable) clayey soils of Puerto Rico (100), and
in ryegrass (Lolium spp. L.) grown on red–brown clayey loam and granite–mica schists in Uganda,
Africa (101). Among the subtropical regions, toxicity has been reported in subtropical United States
in poorly drained soils and soils on limestone (102) and on ultisols. However, the impermeability
of soils does not seem essential for manganese toxicity (103). In southeastern Australia, manganese
toxicity has been reported in fruit trees grown in neutral-pH duplex soils (104), in French beans
(Phaseolus vulgaris L.) grown in manganese-rich basaltic soil (105), and in pasture legumes (106).
There is very little information available on manganese toxicity in temperate regions, though one
report found toxicity on soils characterized by low pH and high concentrations of readily exchange-
able manganese (107).
12.6.2 INDICATOR PLANTS
A number of crops are considered sensitive to manganese toxicity, and these include alfalfa, cabbage,
cauliflower (Brassica oleracea var. botrytis L.), clover (Trifolium spp. L.), pineapple (Ananas como-
sus Merr.), potato (Solanum tuberosum L.), sugar beet, and tomato (Lycopersicon esculentum Mill.)
(74,108). An excess of one nutrient can aggravate a deficiency of another, and so symptoms of man-
ganese toxicity bear some features of deficiency of another nutrient. Additionally, toxicity of man-
ganese is often confused with aluminum toxicity as both often occur in acid soils. However, in some
species such as wheat (109) and rice (110), the tolerance to these two toxicities is opposite (111).
12.6.3 SYMPTOMS
The visual symptoms of manganese toxicity vary depending on the plant species and the level of
tolerance to an excess of this nutrient. Localized as well as high overall concentrations of man-
ganese are responsible for toxicity symptoms such as leaf speckling in barley (112), internal bark
necrosis in apple (113), and leaf marginal chlorosis in mustard (Brassica spp. L.) (114).
The symptoms observed include yellowing beginning at the leaf edge of older leaves, some-
times leading to an upward cupping (crinkle leaf in cotton, (115)), and brown necrotic peppering on
older leaves. Other symptoms include leaf puckering in soybeans and snap bean (116); marginal
chlorosis and necrosis of leaves in alfalfa, rape (Brassica napus L.), kale (Brassica oleracea var.
acephala DC.), and lettuce (Lactuca sativa L.) (116); necrotic spots on leaves in barley, lettuce, and
soybeans (116); and necrosis in apple bark (i.e., bark measles) (60). Symptoms in soybeans include

chlorotic specks and leaf crinkling as a result of raised interveinal areas (117,118); chlorotic leaf
tips, necrotic areas, and leaf distortion (102) in tobacco (Nicotiana tabacum L.).
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12.6.4 TOLERANCE
Reduction of manganese to the divalent and therefore more readily absorbed form is promoted in
waterlogged soils, and tolerance to wet conditions has coincided with tolerance to excess man-
ganese in the soil solution. Graven et al. (119) suggested that sensitivity to waterlogging in alfalfa
may be partially due to manganese toxicity, and alfalfa has been shown to be more sensitive to man-
ganese toxicity than other pasture species such as birdsfoot trefoil (Lotus corniculatus L.) (120). In
support of this suggestion, several other pasture species have also been reported to have a relation-
ship between waterlogging and manganese toxicity (121,122). For example, manganese-tolerant
subterranean clover (Trifolium subterraneum cv. Geraldton) was reported to be more tolerant to
waterlogging than the manganese-sensitive medic (Medicago truncatula Gaertner) (123). Increased
tolerance to manganese toxicity by rice when compared with soybean is combined with increased
oxidizing ability of its roots (124,125).
Tolerance to manganese toxicity has also been related to a reduction in the transport of man-
ganese from the root to the shoot as shown by comparison between corn (tolerant) and peanut
(Arachis hypogaea L.) (susceptible) (126,127). Furthermore, tolerance to manganese toxicity was
observed in subterranean clover (compared with Medicago truncatula) and was associated with a
lower rate of manganese absorption and greater retention in the roots (123). In an extensive study
comparing eight tropical and four temperate pasture legume species, it was concluded that tolerance
to manganese toxicity was partially attributable to the retention of excess manganese in the root sys-
tem (128). This conclusion was also reached in comparing alfalfa clones that differed in manganese
tolerance (129).
In rice, tolerance to high concentrations of manganese is a combination of the ability to with-
stand high internal concentrations of manganese with the ability to oxidize manganese, thus reduc-
ing uptake. This is in comparison with other grasses that are unable to survive the high
concentrations found in rice leaves (130).
Tolerance is also affected by climatic conditions such as temperature and light intensity (131). For

example, when comparing two soybean cultivars, Bragg (sensitive) and Lee (tolerant), an increase
from 21 to 33ЊC day temperature and 18 to 28ЊC night temperature prevented the symptoms of man-
ganese toxicity in both cultivars, despite the fact that manganese uptake was increased (132,133).
12.7 MANGANESE AND DISEASES
The manganese status of a plant can affect, and be affected by, disease infection, often leading to
the misdiagnosis of disease infection as manganese deficiency or toxicity (134). The manganese
concentration in diseased tissues has been observed to decrease as the disease progresses (135).
This occurrence may be due to the pruning of the root system in the case of root pathogens, lead-
ing to a reduction in the absorptive surface with a resultant decrease in the plant concentration
(136,137). Additionally, microbially induced changes in manganese status, such as that caused by
the grey-speck disease (manganese deficiency) of oats have been reported to be due to the oxidiz-
ing bacteria in the rhizosphere causing the manganese to become unavailable (138,139). Manganese
concentration at the site of infection also has been reported to increase, in direct contrast to the over-
all manganese plant concentration, which has decreased (140).
The most notable interaction between disease and manganese is that of the wheat disease take-
all caused by the pathogen Gaeumannomyces graminis var. tritici, commonly referred to as Ggt.
The importance of manganese in the defence against infection by Ggt was demonstrated by Graham
(23). Manganese is the unifying factor in the susceptibility of varieties to Ggt under several soil con-
ditions, including changing pH and nitrogen forms as shown in a table by Graham and Webb (141).
The role of manganese fertilizer in the amelioration of Ggt has been reported in numerous papers
(137,142,143). The effect of manganese fertilizer on infection by Ggt has been shown to impact
before the onset of foliar symptoms (137,142).
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358 Handbook of Plant Nutrition
TABLE 12.1
List of Critical Concentrations of Manganese in Various Agricultural Crops
Concentration of
Growth Plant Type of
Manganese (mg kg

ϪϪ
1
)
Stage Part Culture Deficient Adequate Toxic Reference Comments
Barley
(
Hordeum vulgare
L.)
45 DAS WS Soil 13–21 24–50 149 Critical estimated at
∼85% max. shoot yield
FS 5–6 WS Literature review 30–100 150 Winter and summer
barley
FS 7–8 WS Literature review 25–100 150 Winter and summer
barley
FS 10 WS Soil Ͻ140 Ͼ190 151 H. distichon
FS 10.1 WS Literature review Ͻ5 25–100 152
Mid to late YMB Field, survey Ͻ12 25–300 700 153
tillering
Veg. YEB Field, soil 12 154 Critical concentration
Black gram
(
Vigna mungo
Hepper)
25–33 DAT WS Solution culture 345–579 155 cv. Regur
Canola
(
Brassica napus
L.)
Veg. ML Literature review 40–100 150 Brassica napus var.
napobrassica

Pre-anthesis YML Literature review 30–250 530–3650 153 Brassica napus,
B. campestris
Early-anthesis YML Literature review 30–100 150 Brassica napus var.
oliefera
Unknown YML Literature review 10 30 156
Cassava
(
Manihot esculentum
Crantz)
30 DAS WS FSC 140–170 157 Toxic criteria at 90%
max. yield
63 DAS YMB Solution culture Ͻ14 158 Critical at 90% max.
yield
Veg. YMB Field Ͻ50 50–250 Ͼ1000 159
3–4 months YMB Field Ͻ45 50–120 Ͼ250 160
Cereal rye
(
Secale cereale
L.)
Young plants WS Survey 200 161 Critical for acidic soils
with pH values 4.1–4.4
22 DAS WS Soil 18–69 162 cv. did not respond to
applied Mn, where
other cereals did
Unknown WS Literature review 14–45 163
FS 5–6 WS Literature review 25–100 150
FS 7–8 WS Literature review 20–100 150
Chickpea
(
Cicer arietinum

L.)
Veg. YML Literature review 60–300 153
Cotton
(
Gossypium hirsutum
L.)
35 DAS WS Soil 494 164
Before anthesis YMB Survey, diag. 50–350 165
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Manganese 359
TABLE 12.1 (
Continued
)
Concentration of
Growth Plant Type of
Manganese (mg kg
ϪϪ
1
)
Stage Part Culture Deficient Adequate Toxic Reference Comments
36 DAS YMB RSC 2–8 11–247 166,167 Critical at 90% max.
yield
Veg. to YMB Survey, Diag. 8 25–500 4000 153
anthesis
Anthesis to YML Literature review 35–100 150
boll develop.
33 DAS 3 YML Soil 49–57 568–689 168 Data for 11 cotton
genotypes
18 DAS YL Solution culture 55 962–3300 169 cv. 517
18 DAS YL Solution culture 45 1580–2660 169 cv. 307

21 DAT 3 young RSC 200–270 4030–10570 170 3 cultivars; peroxidase
leaves activity in leaves
(width Ͻ1 cm) separated Mn toxic
from adequate
Cowpea
(
Vigna unguiculata
Walp.)
25–33 DAT WS Solution culture 79–299 155 Data for 2 cv.
35 DAS WS Field Ͻ1000 Ͼ2000 171 43 cv. examined; toxic
at 50% max. yield
Pre-anthesis YMB Survey, diag. 70–300 153
20 DAT YMB Solution culture 68 172 cv. TVu91, sensitive to
Mn toxicity; symptoms
in old leaves only
20 DAT Old LB Solution culture 183 310 172 cv. TVu91, sensitive to
Mn toxicity; symptoms
in old leaves only
Faba bean
(
Vicia faba
L.)
Unknown YL Literature review 3.3 55 173 Adequate plants no
symptoms
Unknown WS Literature review 109 1083 173
Onset of YML Literature review 40–100 150
anthesis
Early YML Literature review 50–300 1000–2020 153
anthesis
Field pea

(
Pisum sativum
L.)
Unknown YL Literature review 4.2 60–65 173 cv. Wirrega and
Dinkum; adequate
plants no symptoms
Unknown WS Literature review 85 1743–2988 173 cv. Wirrega and
Dinkum; adequate
plants no symptoms
Onset of YML Literature review 30–100 150
anthesis
Pre-anthesis YML Literature review 30–400 Ͼ1000 153
First bloom YML Literature review 25–29 30–400 163
Unknown LB Field 6–13 30–60 86
Continued
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TABLE 12.1 (
Continued
)
Concentration of
Growth Plant Type of
Manganese (mg kg
ϪϪ
1
)
Stage Part Culture Deficient Adequate Toxic Reference Comments
Ginger
(
Zingiber officinale
Roscoe)

2–3 months Upper LB Solution culture 20–23 125–250 950–990 174
2–3 months Lower LB Solution culture 20–23 Յ820 950–990 174
Green gram
(
Vigna radiata
R. Wilcz.)
25–33 DAT WS Solution culture 247–259 784–901 155 cv. Berken
40 DAS YML Soil 20–38 175 cv. ML131; study on
14 soils
Guar
(
Cyamopsis tetragonoloba
Taub.)
25–33 DAT WS Solution culture 92–100 155 cv. Brooks
Hops
(
Humulus lupulus
L.)
Mid season YML Literature review 30–100 150
Kenaf
(
Hibiscus cannabinus
L.)
Maturity Stem Literature review 14–23 163
Linseed, Anthesisax
(
Linum usitatissimum
L.)
70 DAS YL Soil 56 1015 176
Onset of Upper third Literature review 30–100 150

anthesis of shoots
49–70 DAS WS Soil 5–50 500–2000 176
63 DAS WS Soil 14–18 108–145 176
63 DAS WS Field 108–449 176
70 DAS WS Soil 34 2295 176
Lupin
(
Lupinus angustifolius
L.
, L. albus
L.
, L. cosentinii
Guss.)
40 DAS WS Literature review 277 Ͼ6164 177
40 DAS WS Soil 245 Ͼ7724 177 L. albus
40 DAS WS Soil 277 Ͼ6164 177
56 DAS WS Survey 31–55 318–1300 178
Up to early YFEL Soil Ͻ30 153,179 Diagnostic for
anthesis shoot DW
Pre-anthesis YML Literature review 50–1200 1900–16000 153 Three Lupinus spp.
28 DAS YOL Literature review 5.6 245 Ͼ7724 177 L. albus
Anthesis WS Soil, field Ͼ20 179 Predictive for absence
of ‘split seed’ disorder.
Buds and leaves poor
predictors.
Maturity Seed Survey 4–9 7–53 178
Maize; corn
(
Zea mays
L.)

30–45 DAE WS Unknown 50–160 180
Six-leaf stage WS Field 8–9 181
40–60 cm tall YMB Literature review 40–100 150
Tassell— Ear leaf Field, diag. Ͻ15 20–200 3000 153 Symptoms shown in
initial silk toxic range
Initial silk Ear leaf Literature review 10–19 20–200 163
Early silk Ear leaf Field Ͻ11 182
Early silk Ear leaf Field Ͻ11 181 Critical at 90% max.
grain yield
360 Handbook of Plant Nutrition
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TABLE 12.1 (
Continued
)
Concentration of
Growth Plant Type of
Manganese (mg kg
ϪϪ
1
)
Stage Part Culture Deficient Adequate Toxic Reference Comments
Silk Ear leaf Field Ͻ15 20–150 Ͼ200 183
40–60 cm tall Leaf opposite Literature 35–100 150
ear review
Before tassell Leaf below Literature Ͻ15 15–300 163
whorl review
Before tassell Leaf below Field, survey, 20–300 165
whorl diag.
Navy bean
(

Phaseolus vulgaris
L.)
Veg. YML Literature review 20–100 184
60 DAS YMB Survey Ն760 185 Plants with symptoms
had highest levels of
Fe and Mn.
Onset of YML Literature review 40–100 150
anthesis
Unknown YML Literature review 15–49 50–300 163
Oats
(
Avena sativa
L.)
Young plants WS Survey Ͼ300 161 Critical for acidic soils
pH Ͻ 4.7
FS 5–6 WS Literature review 40–100 150
FS 7–8 WS Literature review 35–100 150
FS 6 WS Field Ͻ16 186 Critical at 90% max.
grain yield
FS 10 WS Survey Ͻ15 Ͼ30 187
FS 10.1 WS Field, survey Ͻ5 25–100 163,188
Anthesis WS Survey Ͻ14 14–150 189
Mid to late YMB Field, diag. Ͻ12 25–300 700 153 Symptoms present in
tillering toxic range
Pre-head Upper LB Field, survey 25–100 165
FS 10.5 Flag ϩ next Survey Ͻ12–15 190
older LB
Peanut
(
Arachis hypogaea

L.)
25–33 DAT WS Solution culture 100–212 155 cv. Red Spanish
Pre-anthesis/ YMB Survey, diag. 600–800 165
anthesis
Unknown YMB Survey Ͻ10 191
Pre-anthesis YML Survey, diag. 50–300 Ͼ700 153
to anthesis
Anthesis YML Literature review 50–100 150
Anthesis YML Literature review 20–350 192
49 DAS YML Field 7–0 19–39 193 cv. Florunner; critical
and deficient conc.
Relate to plants grown
at pH (water) ϭ 6.8Ϯ0.1
63 DAS YML Field 7–12 26–64 193 cv. Florunner; critical
and deficient conc.
related to plants grown
at pH (water) ϭ 6.8Ϯ0.1
Continued
Manganese 361
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TABLE 12.1 (
Continued
)
Concentration of
Growth Plant Type of
Manganese (mg kg
ϪϪ
1
)
Stage Part Culture Deficient Adequate Toxic Reference Comments

77 DAS YML Field 8–11 34–66 193
91 DAS YML Field 9–11 37–100 193
105 DAS YML Field 9–13 36–115 193
119 DAS YML Field 9–12 33–118 193
90 DAS YML Field 83–170 244–687 194 Data from three sites;
approx. Mn toxic if Ca/Mn
ratio Ͻ80
Pigeon pea
(
Cajanus cajan
Huth.)
Veg. WS FSC 78–300 300 157 cv. Royes
Rice
(
Oryza sativa
L.)
30 DAT WS RSC 57–130 770–7370 195 Adequate range for
plants not affected by
high Mn supply
Tillering WS Unknown 7000 196
Various WS Solution culture Ͻ20 Ͼ2500 197
Panicle YB Survey 252–792 188
initiation
FS 3–5 YMB Field, diag. 40–500 Ͼ5000 153
Before YMB Literature review 40–100 150
anthesis
Safflower
(
Carthamus tinctorius
L.)

70 DAS YOL Field 20–55 198 Predictive for seed yield
70 DAS Upper S Field 3.5–8 198 Predictive for seed yield
70 DAS Upper S Field 3.5–8 198 Predictive for seed yield
75 DAS YOL Field 20–75 198 Predictive for seed yield
75 DAS Upper S Field 3–4 198 Predictive for seed yield
Maturity Seed Field 6.5–8 198 Diagnostic for seed
Sorghum
(
Sorghum bicolor
Moench.)
24 DAS WS Solution culture 24 217 199
35 DAS WS Solution culture Ͼ860 200
GS 2 WS Field 40–150 201
GS 3 WS Sand 40–70 201 Deficient, marginal,
and adequate ranges
Ͻ50%, 50–90%, and
90–100% max. yield,
respectively
GS 3–5 YMB Field 6–100 201
Veg. and Third LB Survey, diag. Ͻ8 15–350 153
early anthesis below head
63 DAS Middle LB Sand 12–15 20–30 202
GS 6 3BBE Field 8–190 201
GS 7–8 3BBE Field 8–40 201
Anthesis YML Literature review 25–100 150
Soybean
(
Glycine max
Merr.) (Growth stages of soybean are as described by Fehr et al. (203))
37 DAE WS Soil 21–44 246–337 204 cv. Bragg

42 DAS WS Soil 13.349.2 205 cv. Bragg
362 Handbook of Plant Nutrition
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TABLE 12.1 (
Continued
)
Concentration of
Growth Plant Type of
Manganese (mg kg
ϪϪ
1
)
Stage Part Culture Deficient Adequate Toxic Reference Comments
Anthesis YMB Diag., Survey Ͻ15 30–100 750–1000 153
36–46 DAS YMB RSC Ͻ11 Ͼ173 85 Seven cvv. compared
Late Anthesis YMB Literature review 30–100 150
Early YMB Field 6–10 15–36 206 Critical conc. varies
anthesis (R2) with soil
Pre-PS YMB Field, survey, 21–100 207
diag.
First pods YMB Field, survey, Ͻ20 208
diag.
Early PF YMB Survey, diag. 30–200 Ͼ500 165
21 DAT YOL Solution culture 10–13 43 402–648 133 cv. Bragg
21 DAT YOL Solution culture 8–13 38 541–686 133 cv. Lee
14 DAT YML first Solution culture 9.5–18.5 33–69 865–1180 209 Data for four cvv.
trifoliate
38 D after YL Sand 103 1530 210 cv. Maple arrow; tmts
tmt imposed imposed at 39 DAS
38 D after Old leaves Sand 144 2780 210 cv. Maple arrow; tmts

tmt imposed imposed at 39 DAS
Unknown Trifoliate leaf Solution culture 9–13 44–69 479–945 211 cv. Williams
Maturity Seed Field 18.2–26.6 212 cv. Essex
Mature LB Leaf Field 10 213 cv. Bragg
Sugar beet
(
Beta vulgaris
L.)
Tenth leaf WS Soil Ͻ35 30–62 214 Critical at 90% yield
Unknown WS Soil Ͼ800 161 Linked with soil acidity
21 DAT YMB Soil, solution culture Ͼ5000 167 Critical at 90% max.
yield
Veg. YMB Literature review 4–20 Ͼ5500 215
Unknown YMB Literature review 4–0 25–360 216 Plant growth less
below critical;
deficient ϭ symptoms
present; adequate ϭ no
symptoms
50–80 DAS Leaf Literature review 10–25 26–360 163
50–60 DAS ML Literature review 35–100 150
Sugar cane
(
Saccharum spp.
L.)
Rapid growth TVD Field, survey 12–100 217–219
Rapid growth TVD Field, survey Ͻ15 20–200 220
Four months Middle leaves Literature review 100–250 150
(mid-portion
less midrib)
Sunflower

(
Helianthus annuus
L.) (Growth stages of sunflower, R1, R2, etc. are as described by Schneiter and
Miller (221))
R-2 YEL Ͻ13 46–80 222 cv. Hysun 31
18–31 DAS WS FSC 5300 157 cv. Hysun 31
Florets Third fourth Diag. 41–850 Ͼ3000 223
about to LB below
emerge flower bud
Continued
Manganese 363
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364 Handbook of Plant Nutrition
TABLE 12.1 (
Continued
)
Concentration of
Growth Plant Type of
Manganese (mg kg
ϪϪ
1
)
Stage Part Culture Deficient Adequate Toxic Reference Comments
Tea
(
Camellia sinensis
O. Kuntze)
At plucking Mature leaves Field, survey Ͻ50 224
Tobacco
(

Nicotiana tabacum
L.)
Anthesis YMB Survey, diag. 30–250 165
Anthesis YMB Field 33–156 225
Veg YML Survey, Diag. 35–350 1290–1420 153
(40–80 DAE)
Various Leaves Various 160 933–11,000 75
Veg. Leaves (all) Solution culture 33 797 226 cv. KY14
Veg. Leaves (all) Solution culture 41 226 cv. T.I.1112
42 DAT Leaves Sand 700–1200 227 D/N temp 22/18ЊC; cv.
Coker 347
42 DAT Leaves Sand 2000–3500 227 D/N temp 26/22ЊC; cv.
Coker 347
42 DAT Leaves Sand 5000–8000 227 D/N temp 30/26ЊC; cv.
Coker 347
Mature Cured leaves Field 115 228 YieldՆ 3.2 t/ha
Mature Cured leaves Sand 7000 229
Triticale
(
X Triticosecale
)
22 DAS WS Soil 11–15 162 Concentration
associated with reduced
growth in two cvv.
25 DAS WS Solution culture 1100–3200 230 Toxic range associated
with plant yield
reduction in four cvv.
Wheat
(
Triticum aestivum

L. and
Triticum durum
Desf.)
18–31 DAS WS FSC 280 157
22 DAS WS Soil 9–12 162 Conc. associated with
plant symptoms and
reduced growth in
seven cvv.
25 DAS WS Soil 6 37–116 139 Three levels of Mn
applied
Mid tillering WS Field 11 23 137 Two levels of Mn
applied
FS 5–6 WS Literature review 35–100 150 Winter and summer
wheats
FS 7–8 WS Literature review 30–100 150 Winter and summer
wheats
FS 10.1 WS Literature review 5–24 25–100 163 Spring wheat
Mid to late YMB Field, survey Ͻ12 25–300 700 223 Toxicity symptoms
tillering observed
Just before Upper two Literature review 16–200 163 Winter
heading leaves wheat
Maturity Grain Field 18.2 231
Maturity Grain Soil Ͻ15.5 Ͼ24 232 Critical at max. grain
yield
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Several mechanisms have been proposed for the interaction between manganese and disease
resistance. These include lignification, with maximal levels reached at the same concentration
of manganese as maximal biomass production (144); the concentration of soluble phenols, where
manganese deficiency leads to a decrease in the their concentration (144); inhibition of aminopep-
tidase, which supplies essential amino acids for fungal growth, under manganese-deficient

conditions (145); inhibition of pectin methylesterase, which is a fungal enzyme for degrading
host cell walls, under manganese-deficient conditions (146); inhibition of photosynthesis leading to
a decrease in root exudates and thus becoming more susceptible to invasion by root pathogens
(142), though this mechanism has been shown not to be important in controlling Ggt by the lack of
effect of foliar-applied manganese (137,147). A plant capable of mobilizing high concentrations of
Mn
2ϩ
that are toxic to pathogens but not to plants in the rhizosphere may directly inhibit pathogenic
attack (141).
12.8 CONCLUSION
This review has focused predominantly on the function of manganese in plants and its concentrations
for maintaining optimal growth; the vast literature on diagnostics is heavily drawn on in Table 12.1.
Developments in the last 10 years in manganese physiology and diagnostics have largely been
refinements on the previous work rather than new radical developments. This may change with the
emerging of new molecular technologies in the area of plant mineral nutrition.
ACKNOWLEDGMENTS
The authors thank Dr. Paul Lonergan for assistance in reviewing this chapter, and Margie Palotta
for the photographs.
Manganese 365
TABLE 12.1 (
Continued
)
Concentration of
Growth Plant Type of
Manganese (mg kg
ϪϪ
1
)
Stage Part Culture Deficient Adequate Toxic Reference Comments
Winged bean

(
Psophocarpus tetragonolobus
DC.)
25–33 DAT WS Solution culture 218–225 155 cv. UPS 31
42 DAS WS Sand 29–49 233
Key
Growth stage
DAE, days after emergence; DAS, days after sowing; DAT, days after transplanting; FS, Feeke’s scale of growth in cereals
defined by Large 1954 (234); GS, growth stage; PF, pod fill/ grain fill; PS, pod set; Veg., vegetative.
Plant part
BBE, blade below ear; L, leaf; LB, leaf blade; ML, mature leaf; Trifol. L., trifoliate leaves; TVD, top visible dewlap (sugar
cane); S, stem; WS, whole shoot; YEL, youngest expanded leaf; YFEL, youngest fully expanded leaf; YL, young leaves; YMB,
youngest mature leaf blade; YML, youngest mature leaf; YOL, youngest open leaf; YOL ϩ1, Next youngest open leaf.
Type of culture
Field, field experiment; sand, sand culture in glasshouse; RSC, solution culture where nutrients were replenished periodi-
cally; diag., diagnostic records from database; soil, soil culture in glasshouse; FSC, flowing solution culture; survey, survey
from commercial crops; solution culture, solution culture in glasshouse.
Source: adapted from D.J. Reuter et al. Plant Analysis: An Interpretation Manual. Collingwood, Vic.: CSIRO Publishing,
1997, pp. 83–284.
CRC_DK2972_Ch012.qxd 7/14/2006 11:19 AM Page 365
REFERENCES
1. R.J. Gilkes, R.M. McKenzie. Geochemistry and mineralology of manganese in soils. In: R.D. Graham,
R.J. Hannam, N.C. Uren, eds. Manganese in Soils and Plants. Dordrecht: Kluwer Academic
Publishers, 1988, pp. 23–35.
2. W. Shi, M. Chino, R.A. Youssef, S. Mori, S. Takagi. The occurrence of mugineic acid in the rhizos-
phere soil of barley plant. Soil Sci. Plant Nutr. 34:585–592, 1989.
3. S.M. Bromfield, R.W. Cumming, D.J. David, C.H. Williams. Change in soil pH, manganese and alu-
minium under subterranean clover pasture. Aust. J. Exp. Agric. Anim. Husb. 23:181–191, 1983.
4. J.T. Sims. Soil pH effects on the distribution and plant availability of manganese, copper and zinc. Soil
Sci. Soc. Amer. J. 50:367–373, 1986.

5. W.L. Lindsay. Inorganic phase equilibria of micronutrients in soils. In: J.J. Mortvedt, P.M. Giordano,
W.L. Lindsay, eds. Micronutrients in Agriculture. Madison, WI: Soil Science Society of America,
1972, pp. 41–57.
6. S.M. Bromfield. The effect of manganese-oxidising bacteria and pH on the availability of manganous
ions and manganese oxides to oats in nutrient solutions. Plant Soil 49:23–39, 1978.
7. S.M. Bromfield, D.J. David. Sorption and oxidation of manganese ions and reduction of manganese
oxide by cell suspension of a manganese-oxidising bacterium. Soil Biol. Biochem. 8:37–43, 1976.
8. N.C. Uren, G.W. Leeper. Microbial oxidation of divalent Mn. Soil Biol. Biochem. 10:85–87, 1978.
9. H.G. Dion, P.J.G. Mann. Three-valent manganese in soils. J. Agric. Sci. 36:239–245, 1946.
10. G.W. Leeper. Six Trace Elements in Soils: Their Chemistry as Micronutrients. Victoria, Australia:
Melbourne University Press, 1970, pp. 20–22.
11. H.M. Reisenauer. Determination of plant-available soil manganese. In: R.D. Graham, R.J. Hannam,
N.C. Uren, eds. Manganese in Soil and Plants. Dordrecht: Kluwer Academic Publishers, 1988, pp.
87–100.
12. P.S. Horstmar. Sur la nutrition de l’avoine, particulierement en ce qui concerne les matieres inor-
ganiques qui sont necessaires a cette nutrition. Ann. Chim. Phys. 32:461–510, 1851.
13. K. Aso. The physiological influence of manganese compounds on plants. Coll. Agric. Imp. Univ.Tokyo
5:177–185, 1902.
14. O. Loew, S. Sawa. The action of manganese compounds on plants. Bull. Coll. Agric. Imp. Univ. Tokyo
5:161–172, 1902.
15. W.E. Brenchley. Inorganic Plant Poisons and Stimulants. Cambridge: The University Press, 1927, pp.
1–134.
16. G. Bertrand. Sur l’internention du manganese dans les oxydations provoquees par lalaccase. Compt.
Rend. Acad. Sci. Paris 124:1032–1355, 1897.
17. G. Bertrand, M. Javillier. Action of manganese and the development of Aspergillus niger. Bull. Soc.
Chim. France 4(IX):212–221, 1912.
18. G. Bertrand, M. Rosenblatt. Sur la présence générale du manganèse dans le règne végétal. Compt.
Rend. 173:333–336, 1921.
19. P. Maze. Oxydation de l’ammoniaque ou nitrification par les vegetaux. Compt. Rend. Soc. Biol. Paris
77:98–102, 1914.

20. J.S. McHargue. The occurrence and significance of manganese in the seed coat of various seeds.
J. Amer. Chem. Soc. 36:2532–2536, 1914.
21. J.S. McHargue. The role of manganese in plants. J. Amer. Chem. Soc.44:1592–1598, 1922.
22. J.N. Burnell. The biochemistry of manganese in plants. In: R.D. Graham, R.J. Hannam, N.C. Uren,
eds. Manganese in Soils and Plants: Dordrecht: Kluwer Academic Publishers, 1988, pp. 125–137.
23. R.D. Graham. Effect of nutrient stress on susceptibility of plants to disease with particular reference
to the trace elements. Adv. Bot. Res. 10:221–276, 1983.
24. J. Amesz. The role of manganese in photosynthetic oxygen evolution. Biochim. Biophys. Acta
726:1–12, 1993.
25. G.T. Babcock. The photosynthetic oxygen-evolving process. In: J. Amesz, ed. New Comparative
Biochemistry: Photosynthesis. Amsterdam: Elsevier Science Publishers, 1987, pp. 125–158.
26. R.C. Prince. Manganese at the active site of the chloroplast oxygen-evolving complex. Trend Biochem.
Sci. 132:491–492, 1986.
27. P.E. Kriedemann, R.D. Graham, J.T. Wiskich. Photosynthetic dysfunction and in vivo changes in chloro-
phyll a fluorescence from manganese-deficient wheat leaves. Aust. J. Agric. Res. 36:157–169, 1985.
366 Handbook of Plant Nutrition
CRC_DK2972_Ch012.qxd 7/14/2006 11:19 AM Page 366
28. C.W. Asling, L.S. Hurley. The influence of trace elements on the skeleton. Clin. Orthop. 27:213, 1963.
29. R.M. Leach. Metabolism and function of manganese. In: A.S. Prasad, D. Oberleas, eds. Trace
Elements in Human Health. New York: Academic Press, 1976, pp. 235–247.
30. L.S. Hurley. Manganese and other trace elements. In: B.A. Bowman, R.M. Russell, eds. Nutrition
Reviews’ Present Knowledge in Nutrition. Washington, DC: Nutrition Foundation, 1976, pp. 345–355.
31. L. Erway, L.S. Hurley, A. Fraser. Congenital ataxia and otolith defects due to manganese deficiency in
mice. J. Nutr. 100:643, 1970.
32. P.S. Papavasiliou, S.T. Miller, G.C. Cotzias. Functional interaction between biogenic amines 3Ј 5Ј
cAMP and manganese. Nature 220:74, 1968.
33. G.C. Cotzias, P.S. Papvasiliou, J. Ginas, A. Steck, S. Ruby. Metabolic modification of Parkinson’s dis-
ease and of chronic manganese poisoning. Ann. Rev. Med. 22:305, 1971.
34. G.C. Cotzias, S.T. Miller, P.S. Papavasiliou, L.C. Tang. Interactions between manganese and brain
dopamine. Med. Clin. North Amer. 60:729, 1976.

35. National Research Council (US). Manganese. Washington DC: National Academy of Sciences, Division
of Medical Sciences Committee on Biological Effects of Atmospheric Pollutants, 1973, pp. 1–191.
36. R.M. Leach. Role of manganese in mucopolysaccharide metabolism. Fed. Proc. Fed. Amer. Soc. Exp.
Biol. 30:991, 1971.
37. I. Fridovich. Superoxide dismutase. Ann. Rev. Biochem. 44:147–159, 1975.
38. J.M. McCord. Iron- and manganese-containing superoxide dismutase: structure, distribution and evo-
lutionary relationships. Adv. Exp. Med. Biol. 74:540, 1976.
39. M.F. Utter. The biochemistry of manganese. Med. Clin. North Amer. 60:713, 1976.
40. H.A. Schroeder, J.J. Balassa, I.H. Tipton. Essential trace elements in man: manganese, a study in
homeostasis. J. Chronic Dis. 19:545–571, 1966.
41. E.R. Page, E.K. Schofield-Palmer, A.J. McGregor. Studies in soil and plant manganese. I. Manganese
in soil and its uptake by oats. Plant Soil 16:238–246, 1962.
42. H.R. Geering, J.R. Hodgson, C. Sdano. Micronutrient cation complexes in soil solution. IV. The chem-
ical state of manganese in soil solution. Soil Sci. Soc. Amer. Proc. 33:81–85, 1969.
43. L.V. Kochian. Mechanism of micronutrient uptake and translocation in plants. In: J.J. Mortvedt, F.R.
Cox, L.M. Shuman, R.M. Welch, eds. Micronutrients in Agriculture. Madison, WI: Soil Science
Society America, 1991, pp. 229–296.
44. D.A. Barber, R.B. Lee. The effect of microorganisms on the absorption of manganese by plants. New
Phytol. 73:97–106, 1974.
45. M.J. Webb, W.A. Norvell, R.M. Welch, R.D. Graham. Using a chelate-buffered nutrient solution to
establish the critical solution activity of Mn
2ϩ
required by barley (Hordeum vulgare L.). Plant Soil
153:195–205, 1993.
46. E.R. Page, J. Dainty. Manganese uptake by excised oat roots. J. Exp. Bot. 15:428–443, 1964.
47. G.W. Garnham, G.A. Codd, G.M. Gadd. Kinetics of uptake and intercellular location of cobalt, man-
ganese and zinc in the estuarine green alga Chlorella salina. Appl. Microbiol. Biotechnol. 37:270–276,
1972.
48. E.V. Maas, D.P. Moore. Manganese absorption by excised barley roots. Plant Physiol. 43:527–530,
1968.

49. E.V. Maas, D.P. Moore, B.J. Mason. Influence of calcium and magnesium on manganese absorption.
Plant Physiol. 44:796–800, 1969.
50. S. Ratkovic, Z. Vucinic. The H
1
NMR relaxation method applied in studies of continual absorption of
paramagnetic Mn
2ϩ
ions by roots of intact plants. Plant Physiol. Biochem. 28:617–622, 1990.
51. D.T. Clarkson. The uptake and translocation of manganese by plant roots. In: R.D. Graham, R.J.
Hannam, N.C. Uren, eds. Manganese in Soil and Plants. Dordrecht: Kluwer Academic Publishers,
1988, pp. 101–112.
52. M. Tester. Plant ion channels: whole-cell and single-channel studies. New Phytol. 114:305–340, 1990.
53. S.D. Tyerman. Anion channels in plants. Ann. Rev. Plant Physiol. Plant Mol. Biol. 43:351–373, 1992.
54. J. Hill, A.D. Robson, J.F. Loneragan. The effect of copper supply on the senescence and retransloca-
tion of nutrients of the oldest leaf of wheat. Ann. Bot. 44:279–287, 1979.
55. B.Radjagukguk. Manganese Nutrition in Lupins: Plant Response and the Relationship of Supply to
Distribution. University of Western Australia, Perth. 1981.
56. R.O. Nable, J.F. Loneragan. Translocation of manganese in subterranean clover. I. Redistribution dur-
ing vegetative growth. Aust. J. Plant Physiol. 11:101–111, 1984.
Manganese 367
CRC_DK2972_Ch012.qxd 7/14/2006 11:19 AM Page 367
57. R.O. Nable, J.F. Loneragan. Translocation of manganese in subterranean clover. II. The effects of leaf
senescence and of restricting supply of manganese to part of a split root system. Aust. J. Plant Physiol.
11:113–118, 1984.
58. F.K. El-Baz, P. Maier, A.H. Wissemeier, W.J. Horst. Uptake and distribution of manganese applied to
leaves of Vicia faba (cv. Herzfreya) and Zea mays (cv. Regent) plants. Zh. Pflansenernahr. Bodenk.
153:279–282, 1970.
59. J.N. Pearson, Z. Rengel. Distribution and remobilisation of Zn and Mn during grain development in
wheat. J. Exp. Bot. 45:1829–1835, 1994.
60. N.J. Grundon, A.D. Robson, M.J. Lambert, K. Snowball. Nutrient deficiency and toxicity symptoms.

In: D.J. Reuter, J.B. Robinson, eds. Plant Analysis: An Interpretation Manual. Collingwood, Vic.:
CSIRO Publishing, 1997, pp. 37–51.
61. S. Ramani, S. Kannan. Manganese absorption and transport in rice. Physiol. Plant 33:133–137, 1987.
62. J.F. Loneragan. Distribution and movement of manganese in plants. In: R.D.Graham, R.J. Hannam,
N.C. Uren, eds. Manganese in Soils and Plants. Dordrecht: Kluwer Academic Publishers, 1988, pp.
113–121.
63. W.V. Single, I.F. Bird. The mobility of manganese in the wheat plant II. Redistribution in relation to
foliar application. Ann. Bot. 22:479–488, 1958.
64. W.V. Single, I.F. Bird. The mobility of Mn in the wheat plant II. Redistribution in relation to man-
ganese concentration and chemical state. Ann. Bot. 22:489–502, 1958.
65. R.J. Hannam, R.D. Graham, J.L. Riggs. Redistribution of manganese in maturing Lupinus angusti-
folius cv. Illyarrie in relation to levels of previous accumulation. Ann. Bot. 56:821–834, 1985.
66. J.N. Pearson, Z. Rengel. Uptake and distribution of
65
Zn and
54
Mn in wheat grown at sufficient and
deficient leves of Zn and Mn. II during grain development. J. Exp. Bot. 46:841–845, 1995.
67. R.J. Hannam, K. Ohki. Detection of manganese deficiency and toxicity in plants. In R.D. Graham, R.J.
Hannam, N.C. Uren, eds. Manganese in Soils and Plants. Dordrecht: Kluwer Academic Publishers,
1988, p. 244.
68. W.L. Lindsay. Chemical Equilibria in Soils. New York: Wiley, 1979, pp. 150–161.
69. M.A. Jauregui, H.M. Reisenauer. Calcium carbonate and manganese dioxide as regulators of available
manganese and iron. Soil Sci. 134:105–110, 1982.
70. R.D. Graham, W.J. Davies, D.H.B. Sparrow, J.S. Ascher. Tolerance of barley and other cereals to man-
genese-deficient soils of South Australia. In: M.R. Saric, B.C. Loughman, eds. Genetic Aspects of
Plant Nutrition. The Hague: Marintus Nijhoff/Dr W Junk Publishers, 1983, pp. 339–345.
71. R.J. Hannam, W.J. Davies, R.D. Graham, J.L. Riggs. The effect of soil- and foliar-applied manganese
in preventing the onset of manganese deficiency in Lupinus angustifolius. Aust. J. Agric. Res.
35:529–538, 1984.

72. H.D. Chapman, G.F.J. Liebig, E.R. Parker. Manganese studies on Californian soils and citrus leaf
symptoms of deficiency. Calif. Citrograph. 24(12):427–454, 1939.
73. H.D. Chapman, G.F.J. Liebig, A.P. Vanselow. Some nutritional relationships as revealed by a study of
mineral deficiency and excess symptoms on citrus. Soil Sci. Soc. Amer. Proc. 4:196–200, 1940.
74. T. Wallace. The Diagnosis of Mineral Deficiencies in Plants by Visual Symptoms: A Color Atlas and
Guide. London: H.M. Stationery Office, 1961. p. 23.
75. C.K. Labanauskas. Manganese. In: H.D. Chapman, ed. Diagnostic Criteria for Plants and Soils.
Riverside, CA: H.D. Chapman, 1966, pp. 264–285.
76. R.E. Lucas, B.D. Knezek. Climatic and soil conditions promoting micronutrients deficiencies in
plants. In: J.J. Mortvedt, P.M. Giordano, W.L. Lindsay, eds. Micronutrients in Agriculture. Madison,
WI: Soil Science Society of America, 1972, pp. 265–288.
77. P.H. Gallagher, T.Walsh. The susceptibility of cereal varieties to manganese deficiency. J. Agri. Sci.
Camb. 33:197–203, 1943.
78. M. Nyborg. Sensitivity to manganese deficiency of different cultivars of wheat, oats and barley. Can.
Plant Sci. 50:198–200, 1970.
79. O. Johansson, E. Ekman. Resultat ov de senasti arens svenska mikroelement-forsok II. Forsok med
mangan. St. Jordbr. Fosr. Medd. 62:91–138, 1956.
80. D. Stenuit, R. Poit. Mangaangebrek en mangaanvergiftiging bij landbouwgewassen. Agric. Heverlee.
8:141–172, 1960.
81. R.D. Graham, W.J. Davies, J.S. Ascher. The critical concentration of manganese in field-grown wheat.
Aust. J. Agric. Res. 36:145–155, 1985.
368 Handbook of Plant Nutrition
CRC_DK2972_Ch012.qxd 7/14/2006 11:19 AM Page 368
82. J.C. Brown, W.E. Jones. Differential response of oats to manganese stress. Agron. J. 66:624–626,
1974.
83. H.H. Glasscock, R.L. Wain. Distribution of manganese in the pea seed in relation to Marsh Spot.
J. Agric. Sci. 30:132–140, 1940.
84. G.H. Walton. The effect of manganese on seed yield and the split seed disorder of sweet and bitter phe-
notypes of Lupinus angustifolius and L. cosentinii. Aust. J. Agric. Res. 29:1177–1189, 1978.
85. K. Ohki, D.O. Wilson, O.E. Anderson. Manganese deficiency and toxicity sensitivies of soybean cul-

tivars. Agron. J. 72:713–716, 1980.
86. T. Batey. Manganese and boron deficiency. Minist. Agric. Fish Food, Great Britain Tech. Bull.
21:137–149, 1968.
87. A.D. Robson, K. Snowball. Nutrient deficiency and toxicity symptoms. In: D.J. Reuter and
J.B. Robinson, eds. Plant Analysis: An Interpretation Manual. Melbourne: Inkata Press, 1986,
pp. 13–19.
88. V. Romheld and H. Marschner. Function of micronutrients in plants. In: J.J. Mortvedt, F.R. Cox, L.M.
Shuman, R.M. Welch, eds. Micronutrients in Agriculture. Madison, WI: Soil Science Society of
America, 1991, pp. 297–328.
89. W.K. Gardner, D.G. Parberry, D.A. Barber. The acquisition of phosphorus by Lupinus albus L. I. Some
characteristics of the soil/root interface. Plant Soil 69:19–32, 1982.
90. G.H. Godo, H.M. Reisenauer. Plant effects on soil manganese availability. Soil Sci. Soc. Amer. J.
44:993–995, 1980.
91. N.C. Uren. Chemical reduction of an insoluble higher oxide of manganese by plant roots. J. Plant Nutr.
4:65–71, 1981.
92. H. Marschner, V. Romheld. In vivo measurement of root-induced pH changes at the soil root interface:
effect of plant species and nitrogen sources. Zh. Pflanzenphysiol. 111:241–251, 1983.
93. R.W. Smiley. Rhizosphere pH as influenced by plants, soils and nitrogen fertilizers. Soil Sci. Soc.
Amer. Proc. 38:795–799, 1974.
94. C.D.J. Raper, S.A. Barber. Rooting systems of soybeans I. Differences in root morphology among
varieties. Agron. J. 62:581–588, 1970.
95. R.D. Graham. Breeding for nutritional characteristics in cereals. Adv. Plant Nutr. 1:57–102, 1984.
96. R.D. Graham. Development of wheats with enhanced nutrient efficiency: progress and potential.
Wheat Production Constraints in Tropical Environments, Proceedings of the CIMMYT/INDP
International Symposium Chiang Mai, Thailand, January 19–23, 1988, pp. 305–320.
97. Reference deleted.
98. R.D. Graham. Genotypic differences in tolerance to manganese deficiency. In: In R.D. Graham, R.J.
Hannam, N.C. Uren, eds. Manganese in Soils and Plants. Dordrecht: Kluwer Academic Publishers,
1988, pp. 261–276.
99. R.S. Beckwith, K.G. Tiller, E. Suwadji. The effects of flooding on the availability of trace metals to

rice in soils of differing organic matter status. In: D.J.D. Nicholas, A.R. Egan, eds. Trace Elements in
Soil–Plant–Animal Systems. New York: Academic Press, 1975, pp. 135–149.
100. F. Abruna, J. Vicente-Chandler, R.W. Pearson. Effects of liming on yields and composition of heavily
fertilized grasses and on soil properties under humid tropical conditions. Soil Sci. Soc. Amer. Proc.
28:657–661, 1964.
101. P.H. Le Mare. Experiments on effects of phosphorus on the manganese nutrition of plants. I. Effects
of monocalcium phosphate and its hydrolysis derivatives on ryegrass grown in two Buganda soils.
Plant Soil 47:593–605, 1977.
102. C.E. Bortner. Toxicity of manganese to Turkish tobacco in acid Kentucky soils. Soil Sci. 39:15–33, 1935.
103. C.D. Foy, T.A. Campbell. Differential tolerances of Amaranthus strains to high levels of aluminium
and manganese in acid soils. J. Plant Nutr. 7:1365–1388, 1984.
104. V.O. Grasmanis, G.W. Leeper. Toxic manganese in near-neutral soils. Plant Soil 25:41–48, 1966.
105. A. Siman, F.W. Cradock, P.J. Nicholls, H.C. Kirton. Effects of calcium carbonate and ammonium sul-
phate on manganese toxicity in an acid soil. Aust. J. Agric. Res. 22:201–214, 1971.
106. A. Siman, F.W. Cradock, A.W. Hudson. The development of manganese toxicity in pasture legumes
under extreme climatic conditions. Plant Soil 41:129–140, 1974.
107. H.J. Snider. Manganese in some Illinois soils and crops. Soil Sci. 56:187–195, 1943.
108. G.D. Sherman. Manganese and soil fertility. In: US Department of Agriculture. The Yearbook of
Agriculture. Washington, DC: The United States Government Printing Office, 1957, pp. 135–139.
Manganese 369
CRC_DK2972_Ch012.qxd 7/14/2006 11:19 AM Page 369
109. C.D. Foy, A.L. Flemming, J.W. Schwartz. Opposite aluminium and manganese tolerances of two
wheat varieties. Agron. J. 65:123–126, 1973.
110. L.E. Nelson. Tolerance of 20 rice cultivars to excess Al and Mn. Agron. J. 75:134–138, 1983.
111. C.D. Foy, B.J. Scott, J.A. Fisher. Genetic differences in plant tolerance to manganese toxicity. In: R.D.
Graham, R.J. Hannam, N.C. Uren, eds. Manganese in Soils and Plants. Dordrecht: Kluwer Academic
Publishers, 1988, p. 294.
112. D.E. Williams, J. Vlamis. The effect of silicon on yield and Mn
54
uptake and distribution in the leaves

of barley plants grown in culture solution. Plant Physiol. 32:404–409, 1957.
113. A.G. Fisher, G.W. Eaton, S.W. Porritt. Internal bark necrosis of Golden Delicious apple in relation to
soil pH and leaf manganese. Can. J. Plant Sci. 57:297–299, 1977.
114. C.H. Williams, J. Vlamis, H. Hall, K.D. Gowans. Effects of urbanization, fertilization and manganese
toxicity on mustard plants. Calif. Agric. 25(11):8–10, 1971.
115. D.C. Neal. Crinkle leaf, a new disease of cotton in Louisiana. Phytopathology 27:1171–1175, 1937.
116. C.D. Foy, R.L. Chanley, M.C. White. The physiology of metal toxicity in plants. Ann. Rev. Plant
Physiol. 29:511–566, 1978.
117. K. Ohki. Manganese deficiency and toxicity levels for ‘Bragg’ soybeans. Agron. J. 68:861–864, 1976.
118. M.B. Parker, H.B. Harris, H.D. Morris, H.F. Perkins. Manganese toxicity of soybeans as related to soil
and fertility treatments. Agron. J. 61:515–518, 1969.
119. E.H. Graven, O.J. Attoe, D. Smith. Effects of liming and flooding on manganese toxicity in alfalfa.
Soil Sci. Soc. Amer. Proc. 29:702–706, 1965.
120. J.L. Dionne, A.R. Pesant. Effects of pH and water regime on the yield and Mn content of lucerne and
birdsfoot trefoil grown in the glasshouse. Can. J. Plant Sci. 56:919–928, 1976.
121. I.J. Finn, S.H. Bourget, K.F. Neielson, B.K. Dow. Effects of different soil moisture tensions on grass
and legume species. Can. J. Plant Sci. 41:16–23, 1961.
122. R.E. Mc Kenzie. Ability of forages to survive early spring flooding. Sci. Agric. 31:358–367, 1951.
123. A.D. Robson, J.F. Loneragan. Sensitivity of annual Medicago species to manganese toxicity as
affected by calcium and pH. Aust. J. Agric. Res. 21:223–232, 1970.
124. Y. Doi. Studies on the oxidising power of roots of crop plants. 2. Interrelation between paddy rice and
soybean. Proc. Crop Sci. Soc. Jpn. 12:14–15, 1952.
125. Y. Doi. Studies on the oxidising power of roots of crop plants. 1. The differences of crop plants and
wild grasses. Proc.Crop Sci. Soc. Jpn. 21:12–13, 1952.
126. R. Benac. Effect of manganese concentration in the nutrient solution on groundnuts (Arachis hypogaea
L.). Oleagineau 31:539–543, 1976.
127. R. Benac. Response of a sensitive (Arachis hypogaea) and a tolerant (Zea mays) species to different
concentrations of manganese in the environment. Can. ORSTOM Ser. 11:43–51, 1976.
128. C.S. Andrew, M.P. Hegarty. Comparative responses to manganese excess of eight tropical and four
temperate pasture legume species. Aust. J. Agric. Res. 20:687–696, 1969.

129. G.J. Ouellette, L. Dessureaux. Chemical composition of alfalfa as related to degree of tolerance to
manganese and aluminium. Can. J. Plant Sci. 38:206–214, 1958.
130. J. Vlamis, D.E. Williams. Manganese and silicon interactions in the Gramineae. Plant Soil 28:31–40, 1967.
131. C.D. Foy. Manganese and plants. In: Manganese. Washington, DC: National Academies of Science,
National Research Council, 1973, p. 191.
132. D.P. Heenan, O.G. Carter. Influence of temperature in the expression of manganese toxicities by two
soybean varieties. Plant Soil 47:219–227, 1977.
133. D.P. Heenan, L.C. Campbell. The influence of temperature on the accumulation and distribution of
manganese in two cultivars of soybean (Glycine max L. Merr.). Aust. J. Agric. Res. 41:835–843, 1990.
134. D.M. Huber. Disturbed mineral nutrition. In: J. Horsfall, E.B. Cowling, eds. Plant Pathology — An
Advanced Treatise. New York: Academic Press, 1978, pp. 163–181.
135. D.M. Huber, N.S. Wilhelm. The role of manganese in resistance to plant diseases. In: R.D. Graham,
R.J. Hannam, N.C. Uren, eds. Manganese in Soils and Plants. Dordrecht: Kluwer Academic
Publishers, 1988, pp. 155–173.
136. N.S. Wilhelm, J.M. Fisher, R.D. Graham. The effect of manganese deficiency and cereal cyst nema-
tode infection on the growth of barley. Plant Soil 85:23–32, 1985.
137. N.S. Wilhelm, R.D. Graham, A.D. Rovira. Application of different sources of manganese sulfate
decreases take-all (Greumannomyces graminis var. tritici). Aust. J. Agric. Res. 39:1–10, 1988.
370 Handbook of Plant Nutrition
CRC_DK2972_Ch012.qxd 7/14/2006 11:19 AM Page 370
138. S.M. Bromfield. The oxidation of manganous ions under acid conditions by an acidophilous actino-
mycete from acid soil. Aust. J. Soil Res. 16:91–100, 1978.
139. N.S. Wilhelm, R.D. Graham, A.D. Rovira. Control of Mn status and infection rate by genotypes of
both host and pathogen in the wheat take-all interaction. Plant Soil 123:267–275, 1990.
140. H. Kunoh, H. Ishizaki, F. Kondo. Composition analysis of “halo” area of barley leaf epidermis incited
by powdery mildew infection. Ann. Phytopath. Soc. Jpn. 41:33–39, 1975.
141. R.D. Graham, M.J. Webb. Micronutrients and disease resistance and tolerance in plants. In: J.J.
Mortvedt, F.R. Cox, L.M. Shuman, R.M. Welch, eds. Micronutrients in Agriculture. Madison, WI: Soil
Science Society of America, 1991, pp. 333–339.
142. R.D. Graham, A.D. Rovira. A role for manganese in the resistance of wheat plants to take-all. Plant

Soil 78:441–444, 1984.
143. A.D. Rovira, R.D. Graham, J.S. Ascher. Reduction in infection of wheat roots by Gaeumannomyces
graminis var. tritici with application of manganese to soil. In: C.A. Parker, ed. Ecology and Management
of Soil-Borne Plant Pathogens. St. Paul, MN: American Phytopathology Society, 1985, pp. 212–214.
144. P.H. Brown, R.D. Graham, D.J.D. Nicholas. The effects of manganese and nitrate supply on the lev-
els of phenolics and lignin in young wheat plants. Plant Soil 81:437–440, 1984.
145. D.M. Huber, R.R. Keeler. Alteration of wheat peptidase activity after infection with powdery mildew.
Proc. Amer. Phytopathol. Soc. 4: 163, 69th Annual Meeting of the American Phytopathological
Society, East Lansing, MI, August 14–18, 1977.
146. T.S. Sadasivan. Effect of mineral nutrients on soil microorganisms and plant disease. In: C.A. Baker,
W.C. Snyder, eds. Ecology of Soil-Borne Pathogens. Proceedings of the International Symposium,
Berkeley: University of California Press, 1965, pp. 460–470.
147. E.M. Reis, R.J. Cook, B.L. McNeal. Effect of mineral nutrition on take-all of wheat. Phytopathology
72:224–229, 1982.
148. D.J. Reuter, D.G. Edwards, N.S. Wilhelm. Temperate and tropical crops. In: D.J. Reuter, J.B.
Robinson, eds. Plant Analysis: An Interpretation Manual. Collingwood, Vic.: CSIRO Publishing,
1997, pp. 83–284.
149. R.L. Bansal, P.N. Takkar, V.K. Nayyar. Critical levels of Mn in coarse textured rice soils in India for
predicting response of barley to Mn application. Fert. Res. 11:61–67, 1987.
150. W.E. Bergmann. Nutritional Disorders of Plants: Development, Visual and Analytical Diagnosis. Jena:
Gustav Fischer, 1992, p. 26.
151. U.C. Gupta. Effect of manganese and lime on yield and on the concentrations of manganese, molyb-
denum, boron, copper and iron in the boot stage tissue of barley. Soil Sci. 114:131–136, 1972.
152. W.C. Dahnke. Barley. In: D.L. Pluncknett, H.B. Sprague, eds. Detecting Mineral Nutrient Deficiencies
in Tropical and Temperate Crops. Boulder, CO: Westview Press, 1989, pp. 81–90.
153. R.G. Weir, G.C. Cresswell. Plant Nutrient Disorders 4. Pastures and Field Crops. Melbourne: Inkata
Press, 1994, pp. 1–126.
154. R.J. Hannam, J.L. Riggs, R.D. Graham. The critical concentration of manganese in barley. J. Plant
Nutr. 10:2039–2048, 1987.
155. R.W. Bell, D.G. Edwards, C.J. Asher. Growth and nodulation of tropical food legumes in dilute solu-

tion culture. Plant Soil 122:249–258, 1990.
156. S. Haneklaus, E. Schnug. Evaluation of the nutritional status of oilseed rape plants by leaf analysis.
Eighth International Rapeseed Congress, Saskatoon, Canada, 1991, pp. 536–541.
157. D.G. Edwards, C.J. Asher. Tolerance of crop and pasture species to manganese toxicity. Ninth
International Colloquium on Plant Analysis and Fertility Problems, Warwick, UK, 1982, pp. 145–150.
158. R.H. Howeler, D.G. Edwards, C.J. Asher. Micronutrient deficiencies and toxicities of cassava plants
grown in nutrient solutions. I. Critical concentrations. J. Plant Nutr. 5:1059–1076, 1982.
159. R.H. Howeler. The mineral nutrition and fertilization of cassava. In: Cassava Production Course. Cali,
Colombia: CIAT, 1978, pp 247–292.
160. R.H. Howeler. Potassium nutrition of cassava. In: R.D. Munson, ed. Potassium in Agriculture.
Madison, WI: American Society of Agronomy, 1985, pp. 819–841.
161. W. Zorn, A. Paraube. Manganese content of cereals, maize and beet as indicator of soil acidity. Zh
Pflanzen Bodenk 156:371–376, 1993.
162. N.E. Marcar, R.D. Graham. Tolerance of wheat, barley, triticale and rye to manganese deficiency dur-
ing seedling growth. Aust. J. Agric. Res. 38:501–511, 1987.
Manganese 371
CRC_DK2972_Ch012.qxd 7/14/2006 11:19 AM Page 371
163. J.B. Jones, Jr., B. Wolf, H.A. MIlls. Plant Analysis Handbook: A Practical, Sampling, Preparation,
Analysis and Interpretation Guide. Athens, GA: Micro-Macro Press, 1991, pp. 1–213.
164. J.C. Brown, W.E. Jones. Fitting plants nutritionally to soils. II. Cotton. Agron. J. 69:405–409, 1977.
165. J.B. Jones, Jr. Plant analysis handbook for Georgia. Univ. Georgia Coll. Agric. Bull. 735, 1974.
166. K. Ohki. Manganese nutrition of cotton under two boron levels. Agron. J. 66:572–575, 1974.
167. K. Ohki, A. Ulrich. Manganese and zinc appraisal of selected crops by plant analysis. Commun. Soil
Sci. Plant Anal. 8:297–312, 1977.
168. C.D. Foy, H.W. Webb, J.E. Jones. Adaptation of cotton genotypes to an acid, manganese toxic soil.
Agron. J. 73:107–111, 1981.
169. C.D. Foy, R.R. Weil, C.A. Coradetti. Differential manganese tolerances of cotton genotypes in nutri-
ent solution. J. Plant Nutr. 18:685–706, 1995.
170. C.W. Kennedy, J.E. Jones. Evaluating quantitative screening methods for manganese toxicity in cot-
ton genotypes. J. Plant Nutr. 14:1331–1339, 1991.

171. B.T. Kang, R.L. Fox. A methodology for evaluating the manganese tolerance of cowpea (Vigna
unguiculata) and some preliminary results of field trials. Field Crops Res. 3:199–210, 1980.
172. A.H. Wissemeier, W.J. Horst. Manganese oxidation capacity of homogenates of cowpea (Vigna
unguiculata L. Walp.) leaves differing in manganese tolerance. J. Plant Physiol. 136:103–109, 1990.
173. K. Snowball, A.D. Robson. Symptoms of Nutrient Deficiencies and Toxicities: Faba Beans and Field Peas.
Perth: University of Western Australia, School of Agriculture, Soil Science, and Plant Nutrition, 1991.
174. C.J. Asher, M.T. Lee. Diagnosis and Correction of Nutritional Disorders in Ginger (Zingiber
officinale). Brisbane: University of Queensland, Department of Agriculture, 1975.
175. R.L. Bansal, V.K. Nayyar. Critical level of Mn in Ustochrepts for predicting response of green gram
(Phaseolus surerus L.) to manganese application. Fert. Res. 21:7–11, 1989.
176. P.J. Hocking, P.J. Randall, A. Pinkerton. Mineral nutrition of linseed and fibre flax. Adv. Agron.
41:221–296, 1987.
177. K. Snowball, A.D. Robson. Symptoms of Nutrient Deficiencies: Lupins. Perth: University of Western
Australia, School of Agriculture, Soil Science, and Plant Nutrition, 1986.
178. M. Perry, J.W. Gartrell. Lupin “split-seed”. A disorder of seed production in sweet, narrow-leafed
lupins. J. Agric. West Aust. 17(4):20–25, 1976.
179. R.J. Hannam, R.D. Graham, J.L. Riggs. Diagnosis and prognosis of manganese deficiency in Lupinus
angustifolius L. Aust. Agric. Res. 36:765–777, 1985.
180. R.B. Lockman. Relationship between corn yields and nutrient concentration in seedling whole-plant
samples. Agronomy Abstracts. Madison, WI: American Society of Agronomy, 1969, p. 97.
181. E. Uribe, D.C. Martens, D.E. Brann. Response of corn (Zea mays L.) to manganese application on
Atlantic costal plain soil. Plant Soil 112:83–88, 1988.
182. H.J. Mascagni, Jr., F.R. Cox. Diagnosis and correction of manganese deficiency in corn. Comm. Soil
Sci. Plant Anal. 15:1323–1333, 1985.
183. J.B. Jones, Jr. Interpretation of plant analysis for several agronomic crops. In: G.W. Hardy, ed. Soil
Testing and Plant Analysis: Part 2. Madison, WI: Soil Science Society of America, 1967, pp. 49–85.
184. R. Hall, H.F. Schwartz. Common bean. In: W.F. Bennett, ed. Nutrient Deficiencies and Toxicities in
Crop Plants. St. Paul, MN: APS Press, 1993, pp. 91–98.
185. K.E. Giller, F. Amijee, S.J. Brodrick, S.P. McGrath, C. Mushi, O.T. Edje, J.B. Smithson. Toxic con-
centrations of iron and manganese in leaves of Phaseolus vulgaris L. growing on freely drained soils

of pH 6.5 in northern Tanzania. Commun. Soil Sci. Plant Anal. 23:1663–1669, 1992.
186. R.E. Karamanos, G.A. Kruger, J.W.B. Stewart. Copper deficiency in cereal and oilseed crops in north-
ern Canadian prairie soils. Agron. J. 78:317–323, 1986.
187. J.K. Hammes, K.C. Berger. Manganese deficiency in oats and correlation of plant manganese with var-
ious soil tests. Soil Sci. 90:239–244, 1958.
188. R.C. Ward, D.A. Whitney, D.G. Westfall. Plant analysis as an aid in fertilizing small grains. In: L.M.
Walsh, J.D. Beaton, eds. Soil Testing and Plant Analysis. Madison, WI: Soil Science Society of
America, 1973, pp. 329–348.
189. C.S. Piper. The symptoms and diagnosis of minor element deficiencies in agricultural and horticultural
crops. I. Diagnostic methods, boron, manganese. Emp. J. Exp. Agric. 8:85–96, 1940.
190. J.W. Martens, R.I.H. McKenzie, V.M. Bendelow. Manganese levels in oats in western Canada. Can J.
Plant Sci. 57:383–387, 1977.
372 Handbook of Plant Nutrition
CRC_DK2972_Ch012.qxd 7/14/2006 11:19 AM Page 372
191. C.I. Rich. Manganese content of peanut leaves as related to soil factors. Soil Sci. 82:353–363, 1956.
192. G.J. Gascho, J.G. Davis. Mineral nutrition. In: J. Smart, ed. The Groundnut Crop. A Scientific Basis
for Improvement. London: Chapman & Hall, 1994, pp. 214–254.
193. M.B. Parker, M.E. Walker. Soil pH and manganese effects on manganese nutrition of peanut. Agron.
J. 78:614–620, 1986.
194. A.W. Bekker, N.V. Hue, L.G.G. Yapa, R.G. Chase. Peanut growth as affected by liming, Ca–Mn inter-
actions, and Cu plus Zn applications to oxidic Samoan soils. Plant Soil 164:203–211, 1994.
195. L.E. Nelson. The effect of temperature regime and substrate manganese on manganese concentration
in rice. J. Plant Nutr. 5:1241–1257, 1982.
196. S. Yoshida. Fundamentals of Rice Crop Science. Los Banos, Laguna, Philippines: International Rice
Research Institute, 1981.
197. A. Tanaka, S.A. Navasero. Manganese content of the rice plant under water culture conditions. Soil
Sci. Plant Nutr. 12:21–26, 1966.
198. D.C. Lewis, J.D. McFarlane. Effect of foliar-applied manganese on the growth of safflower
(Carthamus tinctorius L.) and the diagnosis of manganese deficiency by plant tissue and seed analy-
sis. Aust. J. Agric. Res. 37:567–572, 1986.

199. R.B. Clark, P.A. Pier, D. Knudson, J.W. Maranville. Effect of trace element deficiencies and excesses
on mineral nutrients in sorghum. J. Plant Nutr. 3:357–374, 1981.
200. S. Kuo, D.S. Mikkelsen. Effect of P and Mn on growth response and uptake of Fe, Mn and P by
sorghum. Plant Soil 62:15–22, 1981.
201. R.B. Lockman. Mineral composition of grain sorghum plant samples. III. Suggested nutrient
sufficiency limits at various stages of growth. Commun. Soil Sci. Plant Anal. 3:295–303, 1972.
202. P.N. Takkar, I.M. Chhibba, S.K. Mehta. Twenty Years of Coordinated Research on Micronutrients in
Soils and Plants: 1967–1987. Bhopal, India: IISS.
203. W.R. Fehr, C.E. Caviness, D.T. Burmood, J.S. Pennington. Stage of development descriptions for soy-
beans, Glycine max L. Merrill. Crop Sci. 11:929–931, 1971.
204. J.T. Moraghan, T.P. Freeman, D. Whited. Influence of FeEDHA and soil temperature on the growth of
two soybean varieties. Plant Soil 95:57–67, 1986.
205. R.L. Mikkelsen. Using hydrophilic polymers to improve uptake of manganese fertilizers by soybean.
Fert. Res. 41:87–92, 1995.
206. H.J. Mascagni, Jr., F.R. Cox. Effective rates of fertilization for correcting manganese deficiency in soy-
beans. Agron. J. 77:363–366, 1985.
207. H.G. Small, A.J. Ohlrogge. Plant analysis as an aid in fertilizing soybeans and peanuts. In: L.M.
Walsh, J.D. Beaton, eds. Soil Testing and Plant Analysis. Madison, WI: Soil Science Society of
America, 1973, pp. 315–327.
208. S.W. Melsted, H.L. Motto, T.R. Peck. Critical plant nutrient composition values useful in interpreting
plant analysis data. Agron. J. 61:17–20, 1969.
209. E.O. Leidi, M. Gomez, M.D. de la Guardia. Soybean genetic differences in response to Fe and Mn
activity of metalloenzymes. Plant Soil 99:139–146, 1987.
210. S. Wu. Effect of manganese excess on the soybean plant cultivated under various growth conditions.
J. Plant Nutr. 17:991–1003, 1994.
211. E.O. Leidi, M. Gomez, M.D. de la Guardia. Evaluation of catalase and peroxidase activity as indica-
tors of Fe and Mn nutrition for soybean. J. Plant Nutr. 9:1239–1249, 1986.
212. S.W. Gettier, D.C. Martens, D.L. Hallock, M.J. Stewart. Residual Mn and associated soybean yield
response from MnSO
4

application in a sandy loam soil. Plant Soil. 81:101–110, 1984.
213. K. Ohki. Manganese critical levels for soybean growth and physiological processes. J. Plant Nutr.
3(1–4):271–284, 1981.
214. R.F. Farley, A.P. Draycott. Manganese deficiency of sugar beet in organic soils. Plant Soil.
38(2):235–244, 1973.
215. A. Ulrich, J.T. Moraghan, E.D. Whitney. Sugar beet. In: W.F. Bennett, ed. Nutrient Deficiencies and
Toxicities in Crop Plants. St. Paul, MN: APS Press, 1993, pp 91–98.
216. A. Ulrich, F.J. Hills. Sugarbeets. In: D.L. Plucknett, H.B. Sprauge, eds. Detecting Mineral Nutrient
Deficiencies in Tropical and Temperate Crops. Boulder, CO: Westview Press, 1989, pp 225–240.
217. A.M.O. Elwali, G.J. Gascho. Soil testing, foliar analysis and DRIS as guides for sugarcane fertiliza-
tion. Agron. J. 76:466–470, 1984.
Manganese 373
CRC_DK2972_Ch012.qxd 7/14/2006 11:19 AM Page 373
218. G.J. Gascho, A.M.O. Elwali. Tissue testing of Florida sugarcane. Sug. J. 42:15–16, 1979.
219. D. Bassereau. Sugar cane. In: P. Martin-Prevel, J. Gagnard, P. Gautier, eds. Guide to the Nutrient
Requirements of Temperate and Tropical Crops. New York, USA: Lavoisier Publishing Inc., 1987, pp.
513–525.
220. H. Evans. Elements other than nitrogen, potassium and phosphorus in the mineral nutrition of sugar-
cane. Proc. Int. Soc. Sugar Cane Technol. 10:473–507, 1959.
221. A.A. Schneiter, J.F. Miller. Description of sunflower growth stages. Crop Sci. 21:901–903, 1981.
222. F.P.C. Blamey, R.K. Zollinger, A.A. Schneiter. Sunflower. In: Sunflower Production and Culture.
Madison, WI: American Society of Agronomy, 1997.
223. R.G. Weir. Tissue Analysis for Pastures and Field Crops. Advisory note no. 11/83, NSW Department
of Agriculture, 1983.
224. F.N. Fahmy. Soil and leaf analysis in relation to tree crop nutrition in Papua, New Guinea. In: Abstract
in proceedings of conference on Classification and Management of Tropical Soils. Kuala Lumpur,
1977, pp. 309–318.
225. R.B. Lockman. Mineral composition of tobacco leaf samples. I. As affected by soil fertility, variety
and leaf position. Commun. Soil Sci. Plant Anal. 1:95–108, 1970.
226. J. Wang, M.Y. Nielsen, B.P. Evangelou. A solution culture study of manganese-tolerant and sensitive

tobacco genotypes. J. Plant Nutr. 17:1079–1093, 1994.
227. T.W. Rufty, G.S. Miner, C.D.J. Raper. Temperature effects on growth and manganese tolerance in
tobacco. Agron. J. 71:638–644, 1979.
228. G.K. Evanylo, J.L. Sims, J.H. Grove. Nutrient norms for cured burly tobacco. Agron. J. 80:610–614,
1988.
229. A.D. Johnson, R.W. Knowlton. The effect of manganese on tobacco leaf quality and on the inorganic
cation levels of tobacco leaves. Aust. J. Exp. Agric. Anim. Husb. 10:118–123, 1970.
230. L.M. Mugwira, M. Floyd, S.U. Pate. Tolerances of triticale lines to manganese in soil and nutrient
solution. Agron. J. 73:319–322, 1981.
231. U.C. Gupta. Manganese nutrition of cereals and forages grown in Prince Edward Island. Can. J. Soil
Sci. 66:59–65, 1986.
232. C. Ming,Y. Chungren. Effect of manganese and zinc fertilizer on nutrient balance and deficiency diag-
nosis of winter wheat crops in pot experiment. International Symposium on the Role of Sulphur,
Magnesium, and Micronutrients in Balanced Plant Nutrition, China, 1992, pp. 369–378.
233. A.A. Csizinszky. Influence of total soluble salt concentration on growth and elemental concentration
of winged bean seedlings, Psophocarpus tetragonolobus L. DC. Commun. Soil Sci. Plant Anal.
17:1009–1018, 1986.
234. E.C. Large. Growth stages in cereals. Plant Path. 3:128, 1954.
374 Handbook of Plant Nutrition
CRC_DK2972_Ch012.qxd 7/14/2006 11:19 AM Page 374