Handbook of Plant Nutrition - chapter 12 pptx

Since then, research into the concentrations of manganese that confer de ficiency or toxicity, and the variation between- and within-plant species in their tolerance or susceptibility to

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 De ficiency 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 de ficiency

or toxicity, and the variation between- and within-plant species in their tolerance or susceptibility

to these a fflictions 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

351

attributed to soil conditions Soil pH is one of the most in fluential factors affecting the absorption

of manganese by changing mobility from bulk soil to root surface In addition to research on 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.

man-This chapter reviews literature dealing with the identi fication of manganese deficiency and 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 de ficient, adequate, and toxic concentrations for various crops is included.

tox-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 (MnO2), but lower oxides (Mn2O3, Mn3O4) 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 Mn2 ⫹or Mn3 ⫹ 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 a ffected 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 Mn2 ⫹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) Acidi fication may also inhibit microbial oxidation that is responsible for immobilization of man- ganese Manganese-oxidizing microbes are the most e ffective biological system oxidizing Mn2 ⫹in neutral and slightly alkaline soils (6–8) Relatively, as soil pH increases, chemical immobilization of

Mn2 ⫹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 ESSENTIALITY OFMANGANESE TOHIGHERPLANTS

The first reported investigations into the essentiality of manganese by Horstmar in 1851 (12) 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

suc-(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 INPLANTS

Manganese is involved in many biochemical functions, primarily acting as an activator of enzymes such as dehydrogenases, transferases, hydroxylases, and decarboxylases involved in respiration,

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 O2in chloroplasts (Hill reaction) Owing to the key role

in this essential process, inhibition of photosynthesis occurs even at moderate manganese

de ficiency; however, it does not affect chloroplast ultrastructure or cause chloroplast breakdown until severe de ficiency is reached (27).

lead-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⫺1, with daily intake representing 2

to 5 mg day⫺1in comparison to the body pool of 20 mg (30,40).

12.4 ABSORPTION AND MOBILITY

12.4.1 ABSORPTION MECHANISMS

As mentioned previously, manganese is preferentially absorbed by plants as the free Mn2 ⫹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 Mn2 ⫹and Ca2 ⫹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 ANDMOBILITY OFMANGANESE INPLANTS

The plant part on which symptoms of Mn de ficiency 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 de ficiency 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.

The location of manganese in plants is a signi ficant factor in the expression of deficiency toms and is a ffected 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 e ffect of the variable phloem mobility gives rise to a re- distribution of manganese in plant parts typical of a nutrient with low phloem mobility.

symp-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 ity was given in a study by Nable and Loneragan (57), in which plants provided with an early sup- ply of 54Mn 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.

12.5.2 INDICATORPLANTS

Plants that have been reported to be sensitive to manganese de ficiency 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 de ficiency, with

rye (Secale cereale L.) being the least sensitive However, there seems to be some discrepancy in

the ranking of susceptibility to manganese de ficiency 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 de ficiency, several species previously considered ceptible to manganese de ficiency 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

sus-agreed that grasses (Gramineae, Poaceae), clover (Trifolium spp L.), and alfalfa (Medicago sativa L.)

are not susceptible to manganese de ficiency (76,86).

12.5.3 SYMPTOMS

Characteristic foliar symptoms of manganese de ficiency become unmistakable only when the growth rate is restricted signi ficantly (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

de ficiency (67) Severe necrotic spots or streaks may also form Symptoms often occur first on the middle leaves, in contrast to the symptoms of magnesium de ficiency, 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 als, chlorosis develops first on the leaf base, while with dicotyledons the distal portions of the leaf blade are a ffected first (67).

cere-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 de ficiency 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 de ficiency 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 con firm manganese deficiency Visual symptoms of manganese de ficiency 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 de ficiency is usually conferred by an ability to extract more efficiently available manganese from soils that are considered de ficient Mechanisms that are involved in the improved extraction of manganese from the soil include the production of root exudates (89–91),

di fferences 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 e fficiency can be utilized

by breeding programs to develop more e fficient varieties (95,96).

Tolerance to manganese de ficiency may be attributed to one or more of the following five tive mechanisms (96):

adap-1 Superior internal utilization or lower functional requirement for manganese.

2 Improved internal re-distribution of manganese.

3 Faster speci fic rate of absorption from low manganese concentrations at the root–soil face.

inter-4 Superior root geometry.

5 Greater extrusion of substances from roots into the rhizosphere to mobilize insoluble ganese utilizing: (i) H⫹; (ii) reductants; (iii) manganese-binding ligands; and (iv) microbial stimulants.

man-FIGURE 12.1 Manganese deficiency on crops: left, garden bean (Phaseolus vulgaris L.) and right, ber (Cucumis sativus L.) (For a color presentation of this figure, see the accompanying compact disc.)

cucum-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 e fficiency 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 PREVALENCE

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 INDICATORPLANTS

A number of crops are considered sensitive to manganese toxicity, and these include alfalfa, cabbage, cauli flower (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 de ficiency of another, and so symptoms of ganese toxicity bear some features of de ficiency 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).

man-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, 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

some-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.).

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 ship between waterlogging and manganese toxicity (121,122) For example, manganese-tolerant

relation-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 ganese from the root to the shoot as shown by comparison between corn (tolerant) and peanut

man-(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 tem (128) This conclusion was also reached in comparing alfalfa clones that di ffered in manganese tolerance (129).

sys-In rice, tolerance to high concentrations of manganese is a combination of the ability to 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).

with-Tolerance is also a ffected 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 33 ⬚C day temperature and 18 to 28⬚C 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 a ffect, and be affected by, disease infection, often leading to the misdiagnosis of disease infection as manganese de ficiency 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 de ficiency) 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 e ffect of manganese fertilizer on infection by Ggt has been shown to impact

before the onset of foliar symptoms (137,142).

TABLE 12.1

List of Critical Concentrations of Manganese in Various Agricultural Crops

Concentration of Growth Plant Type of Manganese (mg kg

⫺

⫺1 ) Stage Part Culture Deficient Adequate Toxic Reference Comments Barley (Hordeum vulgare L.)

∼85% max shoot yield

Black gram (Vigna mungo Hepper)

Canola (Brassica napus L.)

Cassava (Manihot esculentum Crantz)

max yield

yield

Cereal rye (Secale cereale L.)

with pH values 4.1–4.4

applied Mn, whereother cereals did

Chickpea (Cicer arietinum L.)

Cotton (Gossypium hirsutum L.)

TABLE 12.1 ( Continued )

Concentration of Growth Plant Type of Manganese (mg kg

⫺

⫺1 ) Stage Part Culture Deficient Adequate Toxic Reference Comments

from adequate

Cowpea (Vigna unguiculata Walp.)

at 50% max yield

Mn toxicity; symptoms

in old leaves only

Mn toxicity; symptoms

in old leaves only

Faba bean (Vicia faba L.)

symptoms

anthesis

anthesis

Field pea (Pisum sativum L.)

Dinkum; adequateplants no symptoms

Dinkum; adequateplants no symptoms

anthesis

Continued

TABLE 12.1 ( Continued )

Concentration of Growth Plant Type of Manganese (mg kg

⫺

⫺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 ⱕ820 950–990 174

Green gram (Vigna radiata R Wilcz.)

14 soils

Guar (Cyamopsis tetragonoloba Taub.)

Hops (Humulus lupulus L.)

Kenaf (Hibiscus cannabinus L.)

Linseed, Anthesisax (Linum usitatissimum L.)

Lupin (Lupinus angustifolius L., L albus L., L cosentinii Guss.)

Pre-anthesis YML Literature review 50–1200 1900–16000 153 Three Lupinus spp.

of ‘split seed’ disorder.Buds and leaves poorpredictors

Maize; corn (Zea mays L.)

grain yield

TABLE 12.1 ( Continued )

Concentration of Growth Plant Type of Manganese (mg kg

⫺

⫺1 ) Stage Part Culture Deficient Adequate Toxic Reference Comments

Navy bean (Phaseolus vulgaris L.)

had highest levels of

Fe and Mn

anthesis

Oats (Avena sativa L.)

older LB

Peanut (Arachis hypogaea L.)

anthesis

to anthesis

and deficient conc.Relate to plants grown

at pH (water)⫽ 6.8⫾0.1

and deficient conc.related to plants grown

at pH (water)⫽ 6.8⫾0.1

TABLE 12.1 ( Continued )

Concentration of Growth Plant Type of Manganese (mg kg

⫺

⫺1 ) Stage Part Culture Deficient Adequate Toxic Reference Comments

ratio ⬍80

Pigeon pea (Cajanus cajan Huth.)

Rice (Oryza sativa L.)

plants not affected byhigh Mn supply

initiation

anthesis

Safflower (Carthamus tinctorius L.)

Sorghum (Sorghum bicolor Moench.)

and adequate ranges

⬍50%, 50–90%, and90–100% max yield,respectively

early anthesis below head

Soybean (Glycine max Merr.) (Growth stages of soybean are as described by Fehr et al (203))