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 351 CRC_DK2972_Ch012.qxd 7/14/2006 11:19 AM Page 351 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, 352 Handbook of Plant Nutrition CRC_DK2972_Ch012.qxd 7/14/2006 11:19 AM Page 352 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. Manganese 353 CRC_DK2972_Ch012.qxd 7/14/2006 11:19 AM Page 353 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 354 Handbook of Plant Nutrition CRC_DK2972_Ch012.qxd 7/14/2006 11:19 AM Page 354 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.) CRC_DK2972_Ch012.qxd 7/14/2006 11:19 AM Page 355 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.). 356 Handbook of Plant Nutrition CRC_DK2972_Ch012.qxd 7/14/2006 11:19 AM Page 356 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). Manganese 357 CRC_DK2972_Ch012.qxd 7/14/2006 11:19 AM Page 357 358 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 CRC_DK2972_Ch012.qxd 7/14/2006 11:19 AM Page 358 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 CRC_DK2972_Ch012.qxd 7/14/2006 11:19 AM Page 359 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 CRC_DK2972_Ch012.qxd 7/14/2006 11:19 AM Page 360 [...]... Translocation of manganese in subterranean clover I Redistribution during vegetative growth Aust J Plant Physiol 11:101–111, 1984 CRC_DK2972_Ch 012. qxd 368 7/14/2006 11:19 AM Page 368 Handbook of Plant Nutrition 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... applied in studies of continual absorption of paramagnetic Mn2ϩ 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... CRC_DK2972_Ch 012. qxd 372 7/14/2006 11:19 AM Page 372 Handbook of Plant Nutrition 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... stages of sunflower, R1, R2, etc are as described by Schneiter and Miller (221)) R-2 18–31 DAS Florets about to emerge YEL WS Third fourth LB below flower bud Ͻ13 FSC Diag 46–80 41–850 5300 Ͼ3000 222 157 223 cv Hysun 31 cv Hysun 31 Continued CRC_DK2972_Ch 012. qxd 7/14/2006 11:19 AM Page 364 364 TABLE 12. 1 Growth Stage Handbook of Plant Nutrition (Continued ) Plant Part Type of Culture Concentration of Manganese... 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... 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... 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 retranslocation 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... 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 ... 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 Mn2ϩ 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... 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, . 357 CRC_DK2972_Ch 012. qxd 7/14/2006 11:19 AM Page 357 358 Handbook of Plant Nutrition TABLE 12. 1 List of Critical Concentrations of Manganese in Various Agricultural Crops Concentration of Growth Plant Type of. 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. 5.3 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