11. Nutrient Relations

11.1.2.1 Primary Minerals

Minerals—for example, quartz, feldspar and mica—are created during the formation of rocks by crystallisation from molten magma (intrusive and igneous rocks) or by recrystallisation under conditions of high pressures and temperatures (metamorphic rocks) in the upper crust of the Earth. Depending on the chemical composition of the magma (acid to alkaline), and the temperature and pressure in the molten material, rocks of different mineral composition are formed (Fig. 11.1a). Silicates are made of silicon–oxygen tetrahedrons and occur with many different crystal structures, representing the largest proportion of primary minerals in the Earth’s crust (see Blume et al. 2010). Different forms of silicates are distinguished (Table 11.2). In most silicates, Al³⁺ ions replace some of the Si⁴⁺ ions. In addition, Si is able to build Si–Si chains similar to C chains. The Si–Si bonds reduce the number of negative charges. Therefore, these minerals contain a reduced number of positively charged ions (cations) such as K⁺, Na⁺, Mg²⁺ and Ca²⁺. During weathering, replacement of alkaline cations with H⁺ takes place. Cations are released from the mineral matrix and then become available to plants, while the crystal structure loses its geometry and falls apart.

Table 11.2

Tetrahedron structures of primary silicates

Primary silicate	Free charges per tetrahedron	Tetrahedra structure	Minerals
Nesosilicates SiO4 4−	4	Tetrahedra are cation saturated	Olivine (Mg, Fe)2[SiO4]
Sorosilicates Si2O7 6−	3	Few tetrahedra covalently bound	Diopside (Ca, Mg)[Si2O6]
Inosilicates SiO3 2−	2	Tetrahedra form a chain	Augite (Ca, Mg, Fe, Al, Na)[Si2O6]n
Cyclosilicates [Si2O6]1.5−	1.5	Tetrahedral chains form ribbons	Amphibolite (Na, K, Ca, Mg, Fe, Al)(OH4)[Al2–4Si14–12O44] Tourmaline NaMg3Al6[(OH)1(BO3)3 [Si6O18]
Phyllosilicates Si2O5 2−	1	Tetrahedra form layers	Muscovite (KAl2)(OH2)[Si3AlO10] Biotite K(Mg, Fe, Mn)3(OH, F)2[AlSi3O10]
Tectosilicates SiO2	No free charges 1 free charge with Al replacing SiO2		Quartz SiO2 Orthoclase feldspar K[AlSi3O8] Anorthite Ca[Al2Si2O8]

The free charges of various primary silicates, as listed in Table 11.2, are the basis for weathering and cation availability for roots. It is mainly the substitution of Si with Al that determines the actual cation content of the rock and the proportion of elements (Fe) that may be oxidised. A series of increasing stability with weathering (olivine → augite → tourmaline → feldspar → quartz) emerges. Basalt, for example, is much more alkaline than granite—that is, it contains more potassium, calcium and magnesium—and thus it weathers faster.

11.1.2.2 Secondary Minerals

The clay minerals allophane and imogolite are exceptions. They occur exclusively in soils derived from volcanic activity. They have a spherical or tubular structure, and they can adsorb anions in acid soils (e.g. phosphate) in such a tight manner that they are no longer available to plants.

Oxides and hydroxides: In parallel to the breakdown of the Si tetrahedrons during silicate weathering, oxidation of metals contributes to the breakdown of the primary crystal structure. The most important oxides and hydroxides are those of Fe (particularly those of Fe²⁺ to Fe³⁺ or Fe hydroxide) and of Mn and Al. Depending on climatic conditions, these oxides form different types of secondary minerals, which are often responsible for the characteristic colouring of soils. Tropical soils are often bright red as a consequence of haematite (α-Fe₂O₃), while the yellow-brown colour of many soils of the temperate zone is caused by goethite (α-FeOOH).

Depending on the original rock and its “weathering history”, sedimentary deposits have different cation contents. Clay-rich soils possess a greater capacity for exchange of cations than sandy soils not only because of their much larger surface area for ion exchange but also because of the greater number of covalent bonds. Secondary minerals are included in sedimentary rocks; for example, limestone contains also aluminium oxide, iron oxide and manganese (hydr)oxide.

As soils develop from abiotic and biotic processes, it is not surprising that the soil map of the Earth reflects, in principle, the distribution of different types of vegetation on Earth (Fig. 11.2). Clay minerals are particularly important components of soils that are formed as new products of the Si–Al minerals during the course of weathering from silicates. According to the climatic conditions when these clay minerals were formed, these could be layer lattices in which the cations are embedded more or less tightly between the layers of Si tetrahedrons and Al octahedrons.

The cation exchange capacity (CEC) of a soil is a measure of the amount of cations that can be reversibly stored. It is large in clay minerals that swell (e.g. montmorillonite: 80–120 cmol_c kg⁻¹ (c = charge)) and small in non-swelling clay minerals (e.g. kaolinite: 1–10 cmol_c kg⁻¹) (see Box 11.1) (Osman 2013). The chemical composition of the original rock or of the sediments determines the availability of water and nutrients (soil fertility) and thus the type of vegetation. Plant cover may increase the CEC of soils by a factor of 10 by formation of “humus” as a product of incomplete decomposition of organic matter. But even at high humus contents in soil, the chemical composition of the original rock determines the type of humus formed and thus the availability of nutrients in the soil: humus has a potential CEC between 100 and 300 cmol_c kg⁻¹, where “c” expresses the fact that the number of charges is counted depending on the soil pH (Osman 2013). Thus, the availability of cations in the soil affects most ecosystem processes.

11.1.3.1 Nutrient Supply in the Soil Solution

In mineral soils, chemically characterised by the content of alkaline cations (base saturation: e.g. K, Mg and Ca) and physically determined by the texture (particle size distribution), roots act as additional ion exchangers. While cations in the soil are in equilibrium between the exchanger (clay minerals, oxides, humus) and the free soil solution, roots cause chemical imbalances because of active transport processes, which enable plants to take up cations against the concentration gradient. This process is in most cases selective for certain ions. In exchange against cations from the soil, the root actively releases H⁺, HCO₃ ⁻ or organic acids to the soil, which originated from the carbon cycle (Jones et al. 2004). The uptake of alkaline cations in exchange for protons results in acidification of soils. With uptake of anions, alkalinisation of soils may occur. If the vegetation is not managed or harvested, these minerals are returned in the dead biomass to the soil as litter. In agriculture and forestry, nutrients are removed from the soil by harvesting, grazing or use of litter, with the consequence that the chemical conditions in the soil change (acidification of soil water, podzolisation) if the depletion exceeds the resupply by weathering. Deposition into the soil of strong acids from the atmosphere, as a result of air pollution (SO₄ ²⁻, NO₃ ⁻), has an effect similar to that of harvesting of plant material, because the input of these anions is not balanced by cations. Fertilisation and liming of soils balance the loss of cations caused by harvesting or leaching.

Box 11.1: Ion Exchange Capacity of Soils

Soils: Soils are the product of weathering and transportation of original materials of the Earth’s continental land surface by physical and chemical processes and biological agents. They are mixed to different extents with dead organic matter, litter and humus.

Cation exchange capacity (CEC): The CEC is an important measure of the cation availability in soils, giving the number (in moles) of cations that can be adsorbed by a defined quantity of soil (expressed in centimoles of charge per kilogram). The magnitude of the CEC depends on the number of available exchange sites of clay minerals, humus, and (hydr)oxides. The carboxyl-, carbonyl- and enol-groups can adsorb cations only when deprotonated (variable charge), and this depends on the pH. In contrast, a proportion of the exchange sites in the crystal structure of clay minerals occurs by replacement of Si⁴⁺ with cations of lower valence (e.g. Al), which is independent of the soil pH (permanent charge). A distinction is drawn between the potential CEC, which includes all exchangeable cations (protons, Al and basic cations, measured at pH 8, for example) and the effective CEC, which includes the exchangeable basic cations and Al at soil pH (Fig. 11.3). In addition to the CEC, the anion exchange capacity (AEC) is important.

According to their clay and humus contents, soils are distinguished by their potential CEC (Blume et al. 2010):

• Arable fields: marshland (37 cmol_c kg⁻¹), pelosol (22 cmol_c kg⁻¹), black earth (18 cmol_c kg⁻¹), para brown earth (17 cmol_c kg⁻¹)

• Forest: brown earth (60 cmol_c kg⁻¹), pseudogley (15 cmol_c kg⁻¹)

Even though, energetically, uptake of anions and cations is fundamentally different, both ions are taken up via transporters and ion channels (Chap. 7). There are specific interactions between cations and anions; for example, in the presence of Cl⁻, uptake of K⁺ decreases (see Marschner 2012).

11.1.3.2 Ion Uptake by Roots

Roots grow in soils as part of the rhizosphere (see Box 11.2), where decomposition of organic material interacts with ion and water uptake by roots. The root surface is covered by microbial and fungal communities. Water uptake and ion uptake (see Box 11.3) take place primarily through younger parts of the root and near the meristems of emerging adventitious roots. In addition, ions may be taken up or lost via leaves and shoots. Above-ground uptake of ions plays an important role during uptake of air pollutants (Burkhardt et al. 2012; Harrison et al. 2000). Along the root, uptake of nutrients changes with root development, as transport depends on the ion radius and chemical composition. Root uptake occurs either in the cell wall (the apoplast) or in the cytosol (the symplast) (Chap. 7). During radial transport from the soil to the central stele, the apoplast is composed of cell walls of cells outside the endodermis. At the endodermis, all ions must pass through the symplast of specialised transmission cells. Besides this radial transport pathway, uptake of ions may also take place through the meristems, where the endodermis is not yet formed. The partitioning of ion uptake between the symplast and apoplast remains under debate. For water it has been estimated that 10–70% of uptake occurs via the apoplasmatic pathway (White 2012); this flow of water may carry a major fraction of Ca, Na and Al through the apoplast into the xylem, and these ions may accumulate in leaves (White 2012). Nevertheless, for metabolic use, these ions must also enter the symplast. In contrast, uptake and transport of P, K, N and Mg occurs in the symplast. Ion transport decreases when the secondary root cortex is developed.

Box 11.2: The Rhizosphere (Contribution by Else K. Bünemann)

The rhizosphere is defined as the volume of soil around living plant roots that is affected by root activities such as root growth, water and nutrient uptake, and exudation of organic anions. The efflux of carbon from roots via lysates from damaged cells and exudates from intact cells (rhizodeposition) is typically 10–20% of net photosynthetically fixed carbon. This carbon stimulates beneficial or pathogenic microorganisms around the roots; this was first observed by Lorenz Hiltner (1862–1923), who coined the term “rhizosphere effect”. The key players in the rhizosphere include the plant; saprophytic organisms such as bacteria, archaea, fungi and invertebrates; and symbiotic microorganisms such as rhizobia and arbuscular mycorrhizal fungi. The interaction of these key players with each other and with the soil environment is called rhizosphere ecology.

Nutrient uptake by plant roots occurs mainly in the root hair zone and leads to the depletion of nutrients close to the root. The extent of the depletion zone depends on the mobility of the nutrient in the soil. For example, the depletion zone of nitrate may extend 40 mm away from the root, while the depletion zone of phosphate typically extends only 2 mm. Phosphorus uptake in barley has been shown to be positively related to root hair length, indicating the importance of root hairs in nutrient uptake. In addition, arbuscular mycorrhizal fungi can transport phosphorus over a 10–15 cm distance. Root hairs and arbuscular mycorrhizal fungi can also increase the drought resistance of plants.

Changes in pH in the rhizosphere result from the secretion of protons or hydroxide ions by plants when they are taking up an excess of cations or anions, respectively, in order to keep their cytosolic pH constant and balance net charges. Mobilisation of iron by secretion of phytosiderophores can be beneficial not only to the secreting plant but also to a neighbouring plant that cannot produce phytosiderophores but can take up the iron–phytosiderophore complex. Secretion of carboxylates such as citrate and malate in order to solubilise phosphorus is sometimes accompanied by secretion of phenolics and cell wall degrading enzymes, which reduce the microbial degradation of the secreted carboxylate.

Techniques to study the rhizosphere include (1) field approaches, as described in Fig. 11.4; (2) horizontal compartmental systems in which a root mat is typically formed on top of a mesh, allowing sampling of the soil just below the mesh; and (3) rhizoboxes with a transparent window allowing observation of root growth and sampling of soil in defined root zones.

There are multiple interactions between nutrient uptake and the activity of various organs of plants (Fig. 11.5). Clearly, transport and retention of a nutrient do not occur independently of other nutrients and are almost always coupled to the transport of organic substances. Here we use nitrate and its turnover in a simplified model. One way of nitrate uptake starts with CO₂ assimilation in the leaf by the enzyme phosphoenolpyruvate (PEP) carboxylase, which carboxylates pyruvate to malate. Malate is transported with K⁺ via the phloem to the root, and there it is decarboxylated to pyruvate and HCO₃ ⁻. The proton may be excreted and exchanged with nitrate. Uptake of K⁺ occurs simultaneously. Nitrate is transported, together with K⁺ as a cation, via the xylem into the shoot. With the reduction of nitrate, K⁺ is released again and balances the malate transport in the phloem. The ion transporters in the roots are regulated by photosynthesis; increased sucrose concentration in the phloem acts also as a signal for up-regulation of the expression of transporter genes involved in the uptake of nitrate, ammonium and other nutrients (see Lejay et al. (2003); Hammond and White (2008)). Independently of this cycle of potassium, malate may also be formed in the root from starch or via assimilation of CO₂ by PEP carboxylase. Anhydrases also form HCO₃ ⁻, which may then be used to take up nitrate by an antiport (Moroney et al. 2001). As the plant requires more N than K, the soil is also made more alkaline by the nitrate uptake through the exchange with HCO₃ ⁻. This is one pathway of nitrate uptake and, depending on the cation balance, nitrate may also be taken up by a symport of protons.

Analysis of the nutrient balance of the plant shows that a large part of nutrients is continuously exchanged within the plant; that is, ions circulate between the root and the shoot. This applies particularly to individual organs that have a limited life-span. Root tips and leaves are periodically or continuously formed newly, utilised transiently and disposed afterwards. Obviously, leaves are time-limited “machines”. Old leaves are shed in response to decreasing physiological activity, for example, when shaded by new leaves. At the same time, formation and shedding of leaves are mechanisms for acclimation of the whole plant to changing environmental conditions (particularly light). Leaf shedding often also serves other functions, for example, detoxification following excessive uptake of salt (e.g. Na).

The expanding leaf is first a sink for carbohydrates and nutrients. Organic substances are required for the structure of the leaf. In the young state, leaves are thus a carbohydrate sink (Chap. 12); that is, sink leaves import carbohydrates for their growth. The leaf becomes a source leaf only after the development of about a third of the leaf area, exporting carbohydrates for maintenance or growth at other sites. Even before full development of the leaf area, a leaf’s capacity for photosynthesis decreases and finally it becomes unproductive. This process of leaf ageing is modified by environmental conditions, including nutrition and light. In contrast to ageing, senescence is a genetically regulated process of the fully differentiated cell (Guarente and Kenyon 2000; Thomas et al. 2000). Ageing and senescence finally lead to shedding of leaves. However, before shedding, part of the invested resource of nutrients is remobilised and transported back into the plant. Large variations exist between species and between types of nutrients. Thus, the leaf is a “flow-through system” for nutrients, highly adjustable to environmental conditions and the internal requirements of the plant for nutrients. The turnover rate of nutrients in plants may change suddenly, depending on the ontogeny of the whole plant, particularly during the change from vegetative to reproductive growth.

11.2.2.1 Amino Acid Uptake and Nutrition

Amino acids are available from N₂ fixation by nitrogen-fixing bacteria, via the direct degradation of litter or from the soil solution (Wallenda et al. 2000). It is known from laboratory and field experiments that roots are able to take up a broad spectrum of amino acids (Näsholm et al. 2009).

Amino acid uptake by roots is very important, particularly in boreal forests at a low rate of nitrification (Persson et al. 2000). Under these conditions, amino acid uptake via the mycorrhiza supplies the plant with almost all of its N demand. Mycorrhizal fungi are able to excrete proteases and thereby break down proteins from litter and use the resulting amino acids directly (Näsholm et al. 1998; Wallenda et al. 2000). It has been shown (Nordin et al. 2001; Persson et al. 2006) that the uptake of amino acids also takes place in the presence of ammonium and nitrate ions, and may reach the same level in fertile soils and at poor sites (Berthrong and Finzi 2006), even though the relative contribution to the N requirement is lower at fertile sites, as additional ammonium and nitrate are available and are utilised (Schulze et al. 1994; Michelsen et al. 1996).

11.2.2.2 Ammonium Uptake and Nutrition

Ammonium is taken up directly in the area of the root hairs or via mycorrhizae. NH₄ ⁺ would be toxic as an ion because its ionic radius and strength are very similar to those of K⁺. Thus, it could enter the cell instead of K⁺, interfering with the pH regulation of the cell. Therefore, NH₄ ⁺ taken up by the root is not stored or transported but rapidly converted into amino acids via the GOGAT (glutamine oxoglutarate aminotransferase) enzyme system. In this process, NH₄ ⁺ is bound to glutamate, using adenosine triphosphate (ATP). The primary amino acid glutamine is formed, which donates the NH₂ group to oxoglutarate by transamination and thereby regenerates glutamate. GOGAT is the enzyme system that also traps free NH₄ ⁺ ions in all other plant organs.

Ammonium uptake (Fig. 11.8; Marschner 1988) occurs generally as an antiport with protons that are excreted by roots. Uptake of ammonium thus leads to soil acidification. For NH₄ ⁺ assimilation in the root, organic molecules are required to provide the C skeletons. They are derived from sucrose produced in the leaf and transported, via the phloem, into the root. Because free amino acids act osmotically and could interfere with the metabolism, amino acids and amides are transported via the xylem into the leaf or they are incorporated into proteins of growing tissues. Ammonium nutrition is important particularly in acidic soils, where nitrification is inhibited and particular cation deficiencies (e.g. Mg, K) may be triggered or increased because of ionic interactions of Mg²⁺ and NH₄ ⁺.

11.2.2.3 Nitrate Uptake and Nutrition

The same area of the root that assimilates ammonium also takes up nitrate and cations (Fig. 11.5). Some mycorrhiza species also take up nitrate. It is not possible to use nitrate directly in the metabolism. It must first be reduced to –NH₂. Nitrate uptake (Fig. 11.9; Marschner 2012) occurs either together with cations as a symport with protons or in exchange of OH⁻. As the requirement for N is larger than that for alkaline cations, the symport with cations is not unlimited. In this case, nitrate uptake takes place in exchange with HCO₃ ⁻, leading to increased soil pH in the rhizosphere. Conversely, with nitrate deficiency in the soil, nitrate is missing as an anion in the uptake of cations, resulting in uptake of Cl⁻ and SO₄ ²⁻ and leading to root injury.

Physiologically, nitrate is not toxic and thus it may be stored in the root or in the shoot. Nitrate storage in the leaf has a regulatory (signal) effect on C allocation (shoot–root growth) of plants (Scheible et al. 1997a, b; Klein et al. 2000). A high nitrate concentration in the leaf stimulates shoot growth and inhibits root growth by regulating the sugar transport to the root, whereas in the soil it stimulates root growth.

Generally, nitrate transport occurs via the xylem into the storage parenchyma of the stem, or into the leaf where nitrate is initially stored together with cations in the vacuole. This increases the osmotic concentration and the water content of leaves (e.g. in “crunchy” nitrate-fertilised vegetables—mainly salad vegetables). If required, nitrate may be transported back from the vacuole into the cytosol. This occurs in exchange with organic acids formed via PEP carboxylase in the leaf. For some plant species, oxalic acid is transported, in exchange for nitrate, into the vacuole. At high Ca supply, this leads to the formation of Ca oxalate in the vacuole. Because of the low solubility of Ca oxalate, crystals are formed in the vacuole, which may even damage the cell structure (rhaphides, giving the typical taste of rhubarb and banana peel). Nitrate is reduced to nitrite in the cytosol. Since nitrite is toxic, it must be reduced to NH₄ ⁺ rapidly, which is then assimilated by the GOGAT system. The rate of turnover of nitrite reductase is faster than that of nitrate reductase. Some of the cations taken up with nitrate are transported back into the phloem; in particular, K⁺ is relocated into the root, accompanied by associated organic acids. These acids are decarboxylated in the root (e.g. malate) and thus support nitrate uptake.

11.2.2.4 Ammonium Nitrate Nutrition

From the specific effects of ammonium and nitrate uptake, particularly with respect to the cation uptake, it becomes clear that the uptake of ammonium nitrate is most favourable for nutrition. Nutrition with ammonium nitrate:

• Maintains the balance of anions and cations in the plant and in the soil.

• Decouples the uptake of cations and anions from the N nutrition (the N requirement is larger than the requirement for cations).

• Maintains the C/N balance. The relation of nitrate and free amino acids (in the case of ammonium nutrition) to starch is a sensitive indicator of the state of nutrition in the leaf (Fig. 11.10). Large nitrate and amino acid concentrations are always connected and indicate excess fertilisation. In contrast, high starch concentrations in the morning correlate with small nitrate and amino acid concentrations and thus indicate N deficiency. Maximum growth rates are achieved under conditions where the nitrate and starch concentrations safeguard the supply for growth during the night, because growth and thus the N and C requirement continue during the night, although assimilation of N and C requires light.

11.2.2.5 Nitrogen Input from the Atmosphere

Nitrogen-containing air pollutants are taken up as gas (NH₃, NO, NO₂) by the plant via the stomata. NH₃ is more soluble than NO, which in turn is more soluble than NO₂. In the leaf, all gases are immediately assimilated into amino acids. Not only gases but also ions dissolved in rainwater and fog reach the inside of the bark via the medullary rays (Klemm 1989). Dust particles containing Mn are deposited on the outside of the cuticle, catalyse the oxidation of NO₂ and SO₂ to nitrate and sulphate in a surface reaction and thus increase N deposition. Uptake of nitrogen from the atmosphere contributes significantly to the N balance for growth in the canopy of trees (up to 20–40% of the N requirements) (Harrison et al. 2000; Burkhardt et al. 2012).

There is a basic difference between the N uptake via the shoot and that via the root. Uptake of nitrogen via the root is metabolically regulated; that is, the plant takes up nitrogen according to its requirements. In contrast, the plant has no “defence” mechanisms against uptake of NO_x, NO₂ or NH₄ ⁺ via the shoot. In addition, uptake via the shoot occurs in exchange with cations (K, Mg); that is, it is coupled with a loss of cations. Nitrogen nutrition from air pollutants thus may lead to an imbalance in cations, particularly if cation uptake is limited.

N ₂ fixation by endosymbiosis enables species of particular plant families to make use of the atmospheric N₂. The Leguminosae family contains more than 12,000 species, the majority of which live in symbiosis with N₂-fixing soil bacteria called the Rhizobia. This rhizobia–legume symbiosis is estimated to be responsible for up to 60% of biologically fixed nitrogen on land (Chapin et al. 2002). A similar symbiosis between plants and bacteria exists in alder (Alnus sp.) and some Poaceae. Even though Acacia species (Leguminosae) are widely distributed in subtropical arid regions, their N₂ fixation is very low (Schulze et al. 2014). The main amount of biologically fixed nitrogen occurs globally in agricultural crops (soybean: Glycine max) (Fig. 11.11; Chap. 21).

11.3.1.1 Sulphur Metabolism

ATP activates sulphate (Fig. 11.14) and adenosine phosphosulphate (APS) is formed. This substance either is transformed by formation of phosphoadenine phosphosulphate (PAPS) into the sulphate ester metabolism—to give, for example, sulpholipids—or serves as a substrate for sulphur reduction. The reduced sulphur is deposited as thiol groups on C skeletons (usually an amino acid, e.g. glutathione), which are synthesised via a sulphotransferase. The S-reduction occurs in the chloroplast, where ferredoxin transfers the electrons to oxidised sulphur (Brychkova et al. 2012). The —SH group is transferred to O-acetylserine, which is split into acetate and cysteine. Cysteine is the starting point for the formation of all organic molecules with an —SH group and thus makes plants sensitive to heavy metals, particularly Hg (Chap. 7).

11.5.1.1 Function of Magnesium

11.5.1.2 Uptake and Requirement for Magnesium

In the soil, magnesium is bound to the substrate predominantly as an exchangeable cation. Mg²⁺ is a component of primary and secondary minerals (serpentine), from which it is released by weathering. The most important antagonist for Mg²⁺ is Ca²⁺, but also NH₄ ⁺, K⁺, Mn²⁺ and even H⁺ influence the uptake of Mg²⁺. In the plant, magnesium is transported in the xylem and phloem, and the ion is stored in chloroplasts. Remobilisation from ageing leaves occurs.

11.5.1.3 Magnesium Deficiency and Excess

Box 11.5: Interactions of Magnesium, Nitrogen and Aluminium During Forest Decline

Mg deficiency was found to be particularly prominent in combination with forest dieback—the so-called “mountain yellowing”, diagnosed as magnesium deficiency (Zech and Popp 1983). Lange et al. (1989a, b) showed in a simple and impressive experiment that mountain yellowing was not caused by airborne pollutants (SO₂, ozone; Fig. 11.16). On spruce twigs with yellowed needles, buds were either left intact or removed so that no further growth could occur. On twigs on the opposite side of the same branch it was observed later that only the needles on twigs with buds yellowed. In contrast, needles on the twigs without buds were green. The experiment showed that magnesium availability from the xylem was sufficient to fulfil the requirement of a non-growing twig but was inadequate to supply growing twig. From this, the question arose as to what factors control growth. Oren and Schulze (1989) were able to show that there is an interaction with the N supply, with the unregulated uptake of nitrogen having a particular growth effect on the canopy. Uptake via the canopy not only leads to disequilibrium between the N supply and cation uptake but also has the effect of causing cation loss during the uptake of ammonium ions (Klemm 1989). The low supply of magnesium, which trees take up from the soil, is further reduced by an antagonism to ammonium, the main nitrogen form in sulphate-contaminated soils (Kaupenjohann et al. 1989). A high ammonium concentration in the soil solution leads to an exchange of ammonium against Al³⁺ on the clay particles, and to high Al concentrations in soil water, which may lead to root damage (Ulrich 1995).

11.5.2.1 Uptake and Requirement for Calcium

Ca occurs in the soil solution as Ca²⁺. Calcium-rich soils are predominantly found on limestone (Box 11.6). The pH of these soils with almost unlimited CaCO₃ is stabilised by the dissolution of CaCO₃ at about pH 7. In Ca-poor soils, CaCO₃ is quickly consumed because it dissolves easily and is not stable against weathering, so the dissolved Ca²⁺ is bound to the ion exchangers in the soil only after the dissolution of the carbonate. The pH of Ca-poor soils is usually around 5 and may decrease on acidic rocks (shales containing pyrite) to 3.5. Below a pH of 5.5 the chemistry of the soil is increasingly determined by aluminium. Ca²⁺ uptake at the root is antagonistically influenced by other cations, particularly Al at low pH. If Al instead of Ca²⁺ is incorporated into the cell wall, elongation growth is inhibited.

Ca²⁺ uptake balances other anions, particularly nitrate and sulphate. It occurs predominantly at the root tip, where the endodermis is not yet formed. Transport into the xylem via the cell wall is possible. Ca²⁺ is transported in the xylem, but it is absent from the phloem. Because of the high pH in the phloem, Ca²⁺ would react with phosphate, forming insoluble apatite. But Ca²⁺ is transported in the phloem bound to a protein (e.g. calmodulin). Ca²⁺ is stored in cell walls and vacuoles together with malate, where Ca oxalate, Ca sulphate or Ca carbonate may be formed by precipitation. High Ca concentrations also occur in the endoplasmic reticulum.

Ca reaches the leaf in the xylem stream but may be transported out via the phloem only if bound to proteins, resulting in an excess and accumulation of Ca in the leaf over time. This becomes obvious from the Ca content of leaves, which rises with age and is particularly striking in conifers with needles of different ages (Oren et al. 1988).

The function of Ca as a stabiliser of the primary wall, by binding to pectin, becomes important in elongation growth, which essentially depends on the presence of Ca. However, Ca has further functions in growth, ranging from the formation of callose to the secretion of the calyptra and the regulation of geotropism. By forming bridges between phosphate and carboxyl groups of phospholipids, Ca maintains the membrane structure.

11.5.2.2 Calcium Deficiency and Excess

11.5.3.1 Uptake and Requirement for Potassium

Potassium occurs predominantly in silicate rocks and becomes reversibly bound to exchangers in the soil, particularly to clay minerals. Because of its ionic radius, potassium fits optimally into the intermediate layers of clay minerals and is therefore preferentially accumulated there (specific adsorption). In some soils, accumulation of K⁺ in clay minerals that are able to swell results in contraction of these clays, which thus “fix” K⁺ so strongly that it is no longer available for plants. The ionic radius and physical characteristics of K⁺ are similar to those of ammonium, so these two ions are easily interchangeable. An excess of ammonium leads to a loss of K⁺ (and other cations) and if these cations are leached, this stimulates acidification of soils. K⁺ and ammonium are both used to determine the cation concentration of the exchanger.

11.5.3.2 Potassium Deficiency and Excess

11.5.3.3 Potassium Accumulation by Mistletoes

Mistletoes are heterotrophic phloem parasites (leaves without chlorophyll), as well as autotrophic xylem parasites (with green leaves). Xylem parasites have been known for their medicinal use since Hippocrates’s time, and not just since Asterix and Getafix. Their alkaloids and lectins (carbohydrate-binding proteins) have major pharmaceutical relevance in the treatment of tumours (Lev et al. 2011). Mistletoes are of botanical interest (Calder and Bernhardt 1983) as they have a high potassium concentration in their leaves (40 mg g⁻¹). In hyperparasitic plants (mistletoe growing on mistletoe), additional accumulation of K and other cations may occur (157 mg g⁻¹ Na in arid locations) (Ehleringer and Schulze 1985) because the mistletoe takes up the xylem water with the cations that accumulate in the shoot, as there is no connection and recirculation to the host’s phloem. This accumulation of salt can lead to leaf damage and abscission. In mistletoes it is particularly significant that despite the high, almost toxic, ion concentrations, they maintain higher transpiration rates than their hosts (Ehleringer et al. 1985). Thus, mistletoes are not only significant sinks for cations but also water parasites (Glatzel and Geils 2009).

An unusual botanical feature of Australian mistletoes (Fig. 11.17) is that their leaves mimic the shape and form of the host so closely that it is difficult to explain (Calder and Bernhardt 1983). Mistletoes have been identified as keystone species for their habitat (Watson 2009; Watson and Herring 2012). When mistletoes were removed from woodlands, species richness declined by over 20% within 3 years. Beside mistletoe fruits feeding birds directly, the nutrient-rich litter fall from the mistletoes, together with enhanced litter fall from the host trees, changes arthropod communities, extending and increasing their availability for insectivores.