The Rhizosphere
VII. CONCLUSION
Most research on the rhizosphere environment has been forcedly descriptive in the past. Recent advances show that organic compounds present in the rhizo- sphere can have a specific role in plant-micro-organism-soil interactions. More- over, it starts to be elucidated:
1. Why plants release exudates
2 . What environmental factors affect exudation
3. How the release is regulated and affected by changes in microbial ac- 4. How changes in soil microbiota affect the root exudation
tivity and composition
These processes and relationships, however, need to be further investigated.
Signal molecules exchanged between plants and microorganisms have been identified that favor beneficial plant colonization. Some compounds present in
soil, e.g., humic molecules, and nutrients can affect root growth and metabolism through stimulation or inhibition of biochemical reactions or processes of root cells and triggering of specific signal transduction pathways; however, molecular information on how the plant senses the environmental condition of the rhizo- sphere is still lacking.
Molecular analysis of the interaction between plants, microbes, and soil components may help us understand the causal relationships of events taking place in the rhizosphere:Nevertheless, due to the necessity to simplify the experi- mental approaches, we still do not have the complete picture that takes into ac- count the relative weight of each factor.
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Functions of Compounds
Released into the Rhizosphere by Soil-Grown Plants
Nicholas C. Uren
La Trobe University, Bundoora, Victoria, Australia
I. INTRODUCTION
The rhizosphere is defined here as that volume of soil affected by the presence of the roots of growing plants. The overall change may be deemed biological, but chemical, biological, and physical properties of the soil, in turn, are affected.
A multitude of compounds are released into the rhizosphere of plants grown in soil. most of which are organic compounds and are normal plant constituents derived from photosynthesis and other plant processes (Table I ) . The relative and absolute amounts of these compounds produced by plant roots vary with the plant species, cultivars, the age of plant, the environmental conditions-including soil properties particularly, the level of physical, chemical, and biological stress, and so on (l,2,10-13).
An impression one gets from the voluminous literature on the rhizosphere and related topics is that each and every compound released has a specific role or function. However, the reality is that very few proposed effects are established;
some are feasible, and some, probably the majority, must remain speculative and unproven.
It is salutary to read the review of Rovira (14), in which he records signifi- cant progress in the understanding of the rhizosphere, and to learn how his opti- mism, born in the 196Os, was transformed into frustration in the 1990s. Admit- tedly the complexity of the system is great, daunting at times and a source of 19
Table 1 Organic Compounds Released by Plant Roots Sugars and polysaccharides
Arabinose. fructose, galactose, glucose. maltose, mannose, mucilages of various compositions. oligosaccharides, raffinose, rhamnose. ribose. sucrose. xylose a-Alanine, B-alanine, y-aminobutyric. arginine. asparagine. aspartic, citrulline.
Amino acids
cystathionine, cysteine, cystine. deoxymugineic, 3-epihydroxymugineic, glutamine.
glutamic. glycine, homoserine, isoleucine, leucine, lysine, methionine, mugineic.
ornithine. phenylalanine, proline, serine, threonine, tryptophane, tyrosine, valine Organic acids
Acetic, aconitic. ascorbic, benzoic, butyric. caffeic. citric, p-coumaric. ferulic.
fumaric. glutaric, glycolic, glyoxilic, malic. malonic, oxalacetic, oxalic, p-hydroxy benzoic, propionic, succinic, syringic, tartaric, valeric, vanillic
Fatty acids Sterols
Linoleic. linolenic. oleic, palmitic. stearic Campesterol, cholesterol. sitosterol, stigmasterol
p-Amino benzoic acid, biotin, choline, N-methyl nicotinic acid, nlacin, pantothenic.
Growth factors
vitamins B , (thiamine). B? (riboflavin). and B, (pyridoxine) Enzymes
Flavonones and nucleotides
Amylase, invertase. peroxidase, phenolase, phosphatases. polygalacturonasc. protease Adenine. flavonone, guanine. uridinelcytidine
Auxins. scopoletin. hydrocyanic acid, glucosides. glucosides. unidentified ninhydrin- positive compounds, unidentified soluble proteins, reducing compounds, ethanol, glycinebetaine. inositol and myo-inositol-like compounds. AI-induced
polypeptides, dihydroquinone, sorgoleone Miscellaneous
S o r t t w s : Referenccs 1-9.
some frustration, but another source of frustration has been born out of unfulfilled expectations-expectations that were, as it turned out, unrealistically high. A period of rationalization may be arising, since, for example, Vaughan and Ord (IS) prefer to refer to phenolic acids as phytotoxins rather than allelochemicals because the proof of allelopathy is difficult to establish; other authors may not be quite so circumspect. Similarly, Jones et al. (16) state: “Root exudates released into the soil surrounding the root have been implicated in many mechanisms for altering the level of soluble ions and molecules within the rhizosphere, however, very few have been critically evaluated.” Further cautionary statements have
been made (l7-21), and McCully’s rhetorical question “How d o real roots work?” is apt here also (22).
Many of the problems arise out of the extrapolation of what happens in solution cultures to soils. Although solution cultures have served and continue to serve very useful functions in basic research of plant science, they differ from soils in several important ways. The surface area available in soils for processes such as sorption is much greater than in solution cultures, solution cultures are mixed continuously, the microbial ecology differs greatly between the two media, and the status of water and O2 in the two systems is usually quite different.
In this chapter I have taken a somewhat skeptical view of the currently accepted rosy picture so readily painted. The role of the devil’s advocate has been adopted to raise issues that are too readily disregarded or assumed glibly to be true. Although some attention is given to the quantitative aspects of the release of root products, the main purpose is to classify types of root products on the basis of their known properties and perceived roles in the rhizosphere.
Most phytoactive compounds do not persist in soil in a free and active form for very long. yet they have been plausibly implicated, for example, in a mecha- nism of infection or nutrient acquisition; therefore some suitable explanation must be found. The “right set of circumstances” was invoked by Uren and Reisenauer (17) to explain how labile reducing agents may be protected physically from O2 and be directed toward insoluble oxides of Mn. The “right set of circumstances”
may have relevance in other situations, and some possibilities are discussed later i n this chapter.
This chapter considers the various types of root products with a potential functional role in the usually tough environment of soil. Only direct effects of immediate benefit to plant growth-e.g., an increase in nutrient solubility-are considered here. Although root products of a plant species may have a direct effect on important groups of soil organisms, such as rhizobia and mycorrhizae.
their effect on the plant is not immediate; these and aspects related to microbial activity in the rhizosphere are not considered here (see Chaps. 4, 7, and IO). For an extensive and recent review of the microorganisms in the rhizosphere, the reader is referred to Bowen and Rovira (23).
II. ROOT GROWTH, THE RHIZOSPHERE,
AND ROOT PRODUCTS
Roots are linear underground organs of plants that grow through soil with a com- plex architecture, a three-dimensional configuration, which in turn secures the
plant and facilitates the exploitation of soil for nutrients and water (24,25). The complexity of root growth and the architecture of root systems are illustrated in several recent publications (26-28). The pattern of root growth is determined largely by the type of plant and its interaction with soil structure. The growth of roots is such that in soil under ideal conditions, which favor full exploitation of
nutrients and water, roots avoid one another and rarely do neighboring roots
interfere with one another; the heterogeneity of soil structure tends to separate roots spatially (29). Under suboptimal soil conditions, where yield is decreased, any configuration of the root system imposed by the conditions cannot make good the deficit.
The rhizosphere forms around each root as it grows because each root changes the chemical, physical, and biological properties of the soil in its immedi- ate vicinity. The rhizosphere along the axis of each root can be described in terms of the longitudinal and radial gradients that develop as a result of root growth.
nutrient and water uptake, rhizodeposition. and subsequent microbial growth. In solution cultures, some of these gradients tend to be obliterated by the active mixing, such that a phytoactive compound released at one point on the root axis may have an impact on or at another more distal (nearer the root apex) point.
This situation may have little or no relevance for soil-grown plants.
Rhizodeposits stimulate microbial growth because of their high energy and C content, and thus they will tend to decrease the availability of nutrients in the region of the rhizosphere, where they are released from the root. Because the apical regions of the root (i.e., from the root hair zone to the root apex) have extracted most nutrients that are available for uptake before there is extensive colonization of the rhizosphere by saprophytic microorganisms, there is no impact on plant growth, but microbial growth is likely to be limited. Merckx et al. (30) found that microbial growth in the rhizosphere of maize was limited by the deple- tion of mineral nutrients. Similarly i t was found that microbial respiration was not limited in the rhizosphere of winter wheat by available C (31), which, in turn, indicates, as one would expect, that perhaps some other nutrient elenient is limiting. The high C-to-N ratio of root products leads to the suggestion that N may be significant (32); therefore it is not a surprise that rhizodeposition by maize plants enhanced microbial transformations of N i n the rhizosphere. particularly immobilization and denitrification (33). Immobilization of other nutrients Inay also occur but, as suggested above, it may not be a problem for the plant, because root extension and absorption of nutrients occurs at a more rapid rate than the coloniz:ltion of the rhizosphere with competing miCr0OrganiSmS.
High root densities Inay lead to the overlapping of rhizospheres, but not in a consistent way, and extensive overlapping is more likely to be the exception rather than the rule. Some poor soil structures (e.&., cloddiness) Inay Cause clllmp- ing of roots, but such an arrangement would not appear to be the preferred way, and it is unlikely to confer any benefits upon the plant’s growth. And even if there are any benefits, they are not sufficient to make good the decrease in PlaIlt yield brought about by poor structure. Although some of the contrived SYstelns of studying plant root exudates utilize clumping of roots in an attempt to mimic the rhizosphere (e.g., Ref. 34), the effects measured in those systems may reflect
what happens when roots are clumped together, nothing more, and not what hap- pens in more normal and desirable circumstances in soil-grown plants in the field.
A common situation that requires some consideration is the emergence of lateral roots. The apices of these roots must grow through the rhizosphere of the superior axis from which they originate and thus may experience specific effects related to the type of exudates produced by the main axis and the microbial population. If the situation in nonsterile solution cultures has relevance in soil, then the high level of bacterial colonization of the rhizoplane observed near emerging laterals of maize in solution cultures (35) may be significant. However, any effects on the new lateral root apex, which may be significant and quite
specific, have not been investigated.
Root products are all the substances produced by roots and released into the rhizosphere (Table 2) (17). Although most root products are C compounds, they include ions, sometimes 02, and even water. Root products may also be classified on the basis of whether they have either a perceived functional role (excretions and secretions) or a nonfunctional role (diffusates and root debris).
Excretions are deemed to facilitate internal metabolism, such as respiration, while secretions are deemed to facilitate external processes, such as nutrient acquisition.
Both excretion and secretion require energy, and some exudates may act as either.
For example, protons derived from COz production in respiration are deemed excretions, while those derived from an organic acid involved in nutrient acquisi- tion are deemed secretions.
Although root-cap cells may have some function in the rhizosphere (36) and most cell contents are covered by the term root e.nrdute.7, i t is difficult to see how root debris might have a function that directly benefits the growth of
Table 2 Root Products
Product Compound
Root exudates
Diffusates Sugars, organic acids, ammo acids,
water. inorganic ions. oxygen, ribo- flavin. etc.
Excretions Carbon dioxide, bicarbonate ions, pro- Secretions Mucilage, protons, electrons, en-
tons, electrons, ethylene, etc.
zymes, siderophores. allelochemi- cals, etc.
Root debris Root-cap cells, cell contents. etc.