APOPLASM
B. Nitrogen and Potassium 1. Nitrate Assimilation
lics under P-deficient conditions was suggested as another metabolic bypass reac- tion involved in liberation and recycling of Pi in P-starved cells (106). Antibiotic properties of certain phenolic compounds (e.g., isoflavonoids) in root exudates (69) may not only counteract infection by root pathogens but also prevent the microbial degradation of exudate compounds involved in P mobilization (31).
Certain root flavonoids have been identified as signal molecules for spore germi- nation and hyphal growth of arbuscular mycorrhizae, and flavonoids are likely to be important also as signaling compounds for the establishment of ectomy- corrhizae ( 1 3 I , 132) (this subject is reviewed in Chap. 7). Phenolics may further contribute to P mobilization by reduction of sparingly soluble Fell1 phosphates (Fig. S) (3 l ) . The specific release of piscidic acid (p-hydroxyphenyl tartaric acid) from roots of P-deficient pigeon pea (CNjcrn~rs cc+uz L.), which is a strong chela- tor for FeIII, has been related to enhanced mobilization of Fe-phosphates in Alfi- sols ( 133). However, considering the comparatively low exudation rates, piscidic acid may be more relevant as a signaling compound for the establishment of microbial associations (e.g.. arbuscular mycorrhiza (AM), rhizobia).
4. Root-Secretory Phosphohydrolases
Enhanced secretion of acid phosphatases (APase) (24,52,134) and phytases ( 1 35) by plant roots and also by rhizosphere microorganisms (136) under P-deficient conditions may contribute to Pi acquisition by hydrolysis of organic P esters in the rhizosphere (Fig. S), which can comprise up to 30-80% of the total soil phosphorus. In many soils, however, the availability of organic phosphorus seems to be limited mainly by the low solubility of certain P forms, such as Ca- and Fe/Al-phytates, which can make up a major propotion of the soil-organic P ( 137- 139). Beissner ( I 04) reported that oxalic acid in root exudates can contribute to some extent to phytate mobilization in soils. Similarly, in ;I P-deficient sandy soil, more Pi was liberated by simultaneous application of acid phosphatase and organic acids identified in rhizosphere soil solution of Hclkm ltrzcllrlrrrcr than by separate application of organic acids or acid phosphatase, respectively (Fig. 6).
Another limiting factor for phosphatase-mediated P mobilization is the low mo- bility of the hydrolytic enzymes (APase, phytase), mainly associated with the root cell wall and with mucilage in apical root zones (140). An alternative function of root secretory acid phosphatases may be the rapid retrieval of phosphorus by hydrolysis of organic P, which is permanently lost by diffusion or from sloughed off and damaged root cells (Fig. S ) (141).
B. Nitrogen and Potassium
B 0
-
-
H,O APase organic organic acids
(control) acids + APase
1
Figure 6 Water-extractable Pi in a phosphorus-deficient sandy soil from Niger (West
Africa) after separate or simultaneous addition of acid phosphatase and of organic acids detected in the proteoid-rhizosphere soil solution of Hukeu unduluru. Organic acids: malic 7.5 mM; citric 2 mM;fumaric 1 mM,t-aconitic 0.6 mM acid phosphatase: Wheat germ APase according to enzyme activity in rhizosphere soil [0.7 U g soil”].
malate and citrate) seems to be affected by the form of nitrogen supplied as nitrate or ammonium. Generally, exudation of the carboxylates is increased with increasing levels of nitrate in the culture medium. This may be related to the function of car- boxylates in intracellular pH stabilization. Nitrate reduction in roots and in the shoot is stimulated with increasing nitrate supply and results in the production of an equivalent amount of OH-, which is neutralized by increased biosynthesis of organic acids or released into the rhizosphere when produced in the root tissue (143,144). The carboxylate anions can be stored in the leaf vacuoles but are also retranslocated to the roots via phloem transport when the leaf storage capacity is limited. In the root tissue, the carboxylate anions are either metabolized by decar- boxylation or can be released into the rhizosphere (1,144,145).
2.
Ammonium AssimilationExcess uptake of cations over anions as a consequence of increased ammonium supply is balanced by extrusion of protons and by synthesis of carboxylic acids
for pH stabilization in the root tissue. The remaining carboxylate anions are re- quired as acceptors for ammonium assimilation in the roots, which is also associ- ated with the production of protons and decarboxylation of organic acids ( I ) . As a consequence, tissue concentrations and root exudation of carboxylates decline with increased ammonium supply (144).
High nitrogen concentrations inhibit the production and release of isofla- vonoids from lupin roots. Compared with nitrate supply, exudation was strongly enhanced by ammonium application (146). Similarly, the well-known inhibitory effect of nitrogen on nodulation during establishment of the legume-rhizobium symbiosis is mainly caused by nitrate ( 1 47). In the short term, intense rhizosphere acidification induced by NH,' nutrition or low rates of NO3- supply may directly stimulate the release of phenolics and other LMW root exudate compounds as a consequence of an increased electrochemical transmembrane potential gradient but also due to acid-induced impairment of membrane integrity (148) (Table 4).
Since flavonoids have important functions as chemoattractants and nod-gene in- ducers for rhizobia (149), nitrogen effects on nodulation may be explained by differential exudation of these compounds depending on N form supply and the N nutritional status of the plants. Root flavonoids are involved also in pathogen and allelopathic interactions (69,l SO), and these processes might be similarly affected by nutritional modifications in root exudation.
3. Potassium Nutrition
Only limited information is available on effects of potassium (K) supply on root exudation. Increased exudation of sugars, organic acids, and amino acids has
Table 4 Rclease of Reducing Root Exudates (e.g..
Phenolics) by Peanut Plants as Affected by Fe Nutritional Status and Short-Term (10 h) Supply of a
NH,'-I 1 mM1-containing nutrient solution
Reducing substances in the
nutrient solution [nmol caffeic acid equivalents
10 h" g" root fresh weight]
pH of the N form nutrient
in nutrient solution
solution after I O h +Fe -Fe
Control
NO3 -N 5.5 5 28
NH,'-N 3 .Y Y I15
been detected in maize as a response to K limitation (142). This may be related to a K deficiency-induced preferential accumulation of LMW N and C com- pounds at the expense of macromolecules (1). In contrast, Gerke (99) reported enhanced extrusion of protons but a reduction in carboxylate exudation in K- deficient wheat, sugar beet, and oil-seed rape. Soil-extraction experiments with carboxylates, amino acids, and sugars revealed that only citrate applied in extraordi- narily high concentrations [6 mmol g" soil] was effective in K desorption. Thus K mobilization by root exudates was suggested to be of minimal importance (99).