Interactions of P Concentrations and Plants 621 Influence of Soil P Concentration on Plants

P is crucial for several aspects of plant metabolism, especially the energy and sugar metabolism, and several enzymatic reactions, including photosynthesis. Plants have therefore developed mechanisms for the uptake and efficient use of P. Maize plants recycled N quicker from old to young tissue when P is deficient, leading to earlier leaf senescence (Usuda 1995). P-deficient plants invest more resources into root development and therefore have an increased root-to-shoot biomass ratio compared to well-nourished plants. Furthermore, they accumulate more carbohydrates in leaves and allocate more carbon to the roots (Hermans et al. 2006).

Carbohydrates may influence gene expression in plants, thus helping to regulate enzymatic pathways in reaction to mineral deficiencies (Lloyd and Zakhleniuk 2004; Hermans et al. 2006). Müller et al. (2007) found that almost 150 genes in Arabidopsis thaliana were synergistically or antagonistically regulated by P and sugar. In white lupin, addition of sucrose, glucose, or fructose to the growth medium stimulated the accumulation of transcripts of genes essential for P uptake in seedlings grown in the dark with sufficient P (Liu et al. 2005). Interruption of phloem flow or growth in the dark of P-deficient plants reduced the accumulation of these transcripts compared with P-deficient control plants (Liu et al. 2005). Thus, it could be shown that the plant P metabolism is closely linked with and may be controlled by photosynthesis and sugar metabolism.

Plants can react to low P concentrations in their organs by adapting their root system and their exudative behavior. P does not move through the soil by bulk flow, but only by diffusion, which is very slow (10-12 to 10-15 m2 s-1, Schachtman et al. 1998). Thus, the geometry of the root system is crucial. He et al. (2003) described increases in total root length and root fineness of rice roots in soil zones with high P content. In split-root experiments, more roots were grown in the high-P compartment, especially when the other compartment was P deficient (He et al. 2003). The same was found for wheat when P was applied in a vertical strip in one of the compartments. In the first weeks of growth, root growth in this high-P strip was increased by plants supplied with 4 mg P kg-1 soil in the other compartment compared to that of plants supplied with 14 mg P kg-1 soil. After 8 weeks of growth, the plants showed similar root growth in the high-P strip (Ma and Rengel 2008). A. thaliana grew longer (Bates and Lynch 1996) and denser (Ma et al. 2001) root hairs in low-P environments.

Mycorrhiza have been shown to be very important for P uptake (Bolan 1991; van der Heijden et al. 2006). In wheat, the arbuscular mycorrhizal colonization decreased with increasing soil P. It was reduced from 60% of root length colonized at 10 mg P kg-1 soil to 10% at 27 mg P kg-1 soil (Covacevich et al. 2007). This was independent of shoot P contents.

An interesting adaptation of the root system to low P is the formation of cluster roots. As they are an adaptation, but not systematically different from other roots (Skene 2003), we will review the knowledge about the well-studied cluster roots in some detail as an example of root functioning.

Cluster roots have first been described for Proteaceae (Purnell 1960), where root clusters are widespread. Meanwhile, cluster roots have also been identified in several other families, including Betulaceae, Fabaceae, and Cucurbitaceae (Lamont 2003; Shane and Lambers 2005). Cluster roots are an aggregation of increased numbers of hairy branch roots at specific regions along the axis of growing roots (Lamont 2003; Shane and Lambers 2005). Opposite every protoxylem pole in the cluster root region, a rootlet develops (Skene 2003). This may lead to an increase of the surface area of 140 times and of the explored soil volume of 300 times per unit length of root as measured in Leucadendron laureolum (Lamont 1983, 2003).

From the cluster roots, carboxylates are exuded at high rates (Shane and Lambers 2005), leading to an increasing mobility and uptake of P and other nutrients (Gerke et al. 2000). A major factor leading to the formation of cluster roots seems to be the P concentration in the plant, not that in the soil (Shane and Lambers 2005). Furthermore, the P concentration in the shoots has been shown to be more influential than that in the roots of white lupin (Shane et al. 2003a) and Hakea prostrata (Shane et al. 2003b). Different P nutrition of the roots of white lupin in a split-root experiment did not lead to differences in root morphology or exudation in the differently treated halves of the root system (Shane et al. 2003a). However, Shane and Lambers (2005) reported results from split-root experiments with other species that did differ in their efforts on the low- and high-P side: H. prostrata and H. trifurcata developed more cluster roots on the low-P side, while Lupinus pilosus developed more on the high-P side. In the soil, cluster roots have generally been found in nutrient-rich layers, even to a depth of 5 m (Pate et al. 2001).

Next to the amount of P, the chemical form of this nutrient (Lambers et al. 2002; Shu et al. 2005; Shane et al. 2008) and the availability of other nutrients, especially nitrogen, potassium, and iron (Shane and Lambers 2005) affects the formation of cluster roots. It seems to be regulated by several plant hormones. Thus, application of auxin led to the production of cluster roots in white lupin at P concentrations that normally suppress cluster roots (Gilbert et al. 2000; Neumann et al. 2000). Cytokinines might also play a role, as kinetin applied to the growth medium of P-deficient white lupin inhibited the formation of cluster roots (Neumann et al. 2000).

A role of noninvasive microorganisms in cluster formation has been suggested, as the number of formed cluster roots in H. prostrata was increased from none to 160 g-1 root when grown on autoclaved sand with autoclaved or non-autoclaved soil extract, respectively (Lamont and McComb 1974). Auxin-producing bacteria have been found to be more frequent in juvenile and mature cluster roots than in senescent cluster roots (Weisskopf et al. 2005). As auxin induces cluster root formation, there might be an interaction between these bacteria and the roots. However, there were no significant differences in the frequency of auxin-producing bacteria between cluster roots and non-cluster roots (Weisskopf et al. 2005). The exudation of pheno-lics by root clusters has been suggested to inhibit microbial breakdown of the exuded carboxylates (Lambers et al. 2006; Weisskopf et al. 2006). Thus, while the role of bacteria in the formation of cluster roots is still being discussed, there are indications for reciprocal influences between rhizosphere bacteria and cluster roots.

To sum up, several mechanisms exist that allow plants to exploit scarce resources of P. Interestingly, some plant species are able to locally adapt their root system and exudation behavior when they encounter soil areas rich in P (Fransen et al. 1999; Shane and Lambers 2005). Mycorrhiza are also able to react to areas rich in P with increased production of hyphae (St. John et al. 1983; Cavagnaro et al. 2005). In contrast, other species seem to take their shoot P concentrations as a trigger for producing more or less roots, regardless of patchy soil concentrations of this nutrient, or they even produce more cluster roots in low-P areas. Figure 6.1 shows several strategic models for root development in environments with patchy P distribution. A general increase in root production as shown in Fig. 6.1b makes sense when the distribution of P is patchy, but nutrient availability is not severely limiting. This strategy ensures a high probability of accessing high-P areas. It could also allow the

Fig. 6.1 Different plant strategies for dealing with patchy distribution of P in soil: (a) initial situation: random distribution of roots, (b) increased root production, (c) production of cluster roots in high-P environments, (d) production of cluster roots at random. For discussion, see text

exploitation of P in deep soil layers if more roots are developed in greater depths. However, it is very cost-intensive, as a lot of resources need to be used for building roots. Under limiting nutrient supply, plants have been found to use up to 35% of photosynthates for root growth, plus an extra 20% for exudation (Lambers et al. 1998). The strategy shown in Fig. 6.1c is more efficient: Cluster roots are developed in all accessed high-P areas. Soil high-P areas are missed more easily than in the case shown in Fig. 6.1b. Therefore, this P-reactive cluster root formation is the best strategy if high-P areas are encountered regularly, e.g., due to their homogeneous distribution throughout the soil or due to their large size. Figure 6.1d shows a strategy where root clusters are formed independently of the P concentration in the affected soil region, e.g., in reaction to low shoot-P concentrations. This would be advantageous if the distribution of P was relatively homogeneous or if the concentration of P outside of high-P areas would still be worthwhile extracting. It could also be an adaptation to seasonal variation, when the P concentration in the plant decreases just before new sources of P become available.

Although cluster roots form an interesting adaptation, species that do not form clusters generally have the same means of accessing nutrients, albeit not in such a condensed form: They use root growth and branching to access nutrient-rich areas, exudation to increase nutrient availability, and absorption for uptake (Skene 2003).

Thus, the outlined regulating factors and strategies also apply to species that do not form cluster roots. Furthermore, nutrient uplift, i.e., net displacement of nutrients from deep layers to the topsoil (Jobbagy and Jackson 2004), is used by plants to make P more accessible. This leads to the next section, where we discuss the influence of plants on soil P concentrations.

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