APOPLASM
C. Iron
VIII. WATER SUPPLY
axenic conditions (60). Under similar culture conditions, a transient release of organic acids (citric, maleic) was observed after addition of high Cu concentra- tions [50 PM] to the culture medium of sunflower (258), suggesting that stimula- tion of root exudation may be triggered by toxic levels of various metal species, probably as a consequence of impaired integrity of the plasma membrane.
VI. TEMPERATURE
Diffusion-mediated release of root exudates is likely to be affected by root zone temperature due to temperature-dependent changes in the speed of diffusion pro- cesses and modifications of membrane permeability (259,260). This might ex- plain the stimulation of root exudation in tomato and clover at high temperatures.
reported by Rovira (261), and also the increase in exudation of sugars and amino acids in maize, cucumber, and strawberry exposed to low-temperature treatments (S-IO'C), which was mainly attributed to a disturbance in membrane permeabil- ity (259,262). A decrease of exudation rates at low temperatures may be predicted for exudation processes that depend on metabolic energy. This assumption is supported by the continuous decrease of phytosiderophore release in Fe-deficient barley by decreasing the temperature from 30 to 5°C (67).
subsequently released into the dry top soil layer (hydraulic lift) (265). Increased root exudation of carbohydrates under conditions of mild or severe drought stress has been reported for several conifer species (266-268) and was attributed to root damage and increased internal carbohydrate concentrations.
High soil moisture levels or flooding are limiting factors for oxygen supply to the roots. Hypoxia causes a shift from aerobic respiration to fermentation of carbohydrates in the root tissue yielding ethanol, lactic acid, and alanine as the main end products, which can accumulate to phytotoxic levels (123,269,270). At least in some plant species, the release of substantial amounts of lactic acid (123,270) and ethanol (269,271) into the root environment may be involved in detoxification of these metabolites. Also the exudation of sugars and amino acids is frequently enhanced under hypoxic conditions (271-273). Ethanol is a chemo- attractant to plant pathogens (274), and increased exudation in response to hyp- oxia may support pathogenic infections, especially in the presence of other exu- date compounds such as amino acids (271).
IX. ELEVATED CO,
The continuous rise of the atmospheric COr concentration during the last decades, mainly as a consequence of anthropogenic COz production, is likely to affect photosynthesis and plant biomass production (275). Numerous studies have dem- onstrated a stimulation of shoot and root growth in plants exposed to elevated COz concentrations (275,276), but the putative consequences for rhizodeposition and rhizosphere processes are still not clear. Loss of assimilated carbon from maize roots was not affected by increased atmospheric COz levels (277). Simi- larly. “CO? pulse-chase labeling experiments with Plcrntago I c ~ ~ z c c ~ o l u t ~ ~ seedlings revealed that carbon loss from the root system was not changed at elevated COz levels, although shoot-to-root allocation of assimilates was increased (278). In P-deficient white lupin, elevated C O z treatments did not affect the amount of citrate released from cluster roots, but citrate exudation started in earlier stages of proteoid root development, suggesting COz-induced modifications of root car- bohydrate metabolism (36). The phosphatase activity associated with the root surface of Awrln barbatc1 and Brortlm hordecrcw~s was also not changed by ele- vated COz levels (279) but increased on a base of root dry weight and root length in aseptically grown wheat seedlings when the COz treatment was associated with P deficiency (280).
X. FUTURE RESEARCH PERSPECTIVES
During the last two decades, the functional characterization of plant root exudates involved in rhizosphere processes has attracted increased attention. The role of
root exudates in plant-microbial interactions, nutrient acquisition, and plant adap- tations to environmental stress or adverse soil-chemical conditions is not only of scientific interest but also implicates obvious practical aspects associated with
the need for production of healthy crop plants and for sustainable agricultural systems.
From the methodological point of view, a critical reevaluation of the tech- niques employed for collection of root exudates and of the experimental results is indicated for many earlier studies in the light of recent findings demonstrating spatial variation of exudate release along the roots and strong effects of mechani- cal impedance, root injury, microbial turnover in the rhizosphere, and sorption
at the soil matrix on recovery of root exudate compounds. Further miniaturization of sampling procedures and analytical techniques (e.g., use of specific micro- probes for specific compounds, reporter bacteria, microsuction cups, capillary electrophoresis, image analysis, and videodensitometry) should enable nonde- structive measurements of rhizosphere processes at a high scale of resolution.
Much more information is necessary about effects of root exudates at realis- tic rhizosphere concentration levels on mobility and plant availability of nutrients and toxic compounds such as heavy metals and pesticides in soils under different environmental conditions. In this context it is also important to consider the possi- bility of synergistic effects of simultaneous chemical reactions in the rhizosphere, which have been demonstrated, for example, for the Fe deficiency response in nongraminaceaous plants including increased redox potential and increased re- lease of reductants and chelating compounds in the apical root zones stimulated by increased release of protons ( l ) . Other examples are possible effects of tran- sient pH changes in the rhizosphere and the release of phenolic compounds coun- teracting the microbial degradation of root exudates involved in nutrient mobili- zation, increased availability of organic P forms for root secretory phosphatases and phytases mediated by a concomitant release of carboxylates, and effects of rhizosphere pH on metal complexation with organic ligands.
Flavonoids and other phenolic compounds released by plant roots have important functions in plant-pathogenic interactions, feeding deterrence, nema- tode resistance, and allelopathic interactions; they also serve as signal molecules for the establishment of symbiotic associations (72,149). However, a detailed analysis of signaling pathways involved in these interactions is currently available in only a limited number of cases (see also Chap. 7).
Attempts to manipulate root exudation of higher plants by use of genetic engeneering, breeding technologies, or modification of culture conditions to in- crease efficiency for nutrient acquisition, resistance to adverse soil-chemical con- ditions, or designing of plants for phytoremediation and phytomining strategies (281) requires a detailed knowledge of the physiological mechanisms involved in the regulation of root exudation and of the rhizosphere processes as well. Thus, for a better understanding of the complex interactions at the root-soil interface,
a multidisciplinary approach is necessary, integrating the fields of soil chemistry, soil microbiology, plant nutrition, plant physiology, and molecular biology.
ACKNOWLEDGMENTS
The authors wish to thank Mrs. Heidi Jane Hawkins for critically reading the manuscript.
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