Mechanisms for Enhanced Phosphorus Uptake in Low P Soils

Even in very fertile soils, phosphorus concentrations in the soil solution are low, rarely exceeding 10 /¿M. This is several orders of magnitude lower than the concentration of phosphorus in plant tissues, typically 5-20 mM (Marschner, 1995; Raghothama, 1999). It is therefore not surprising that plants have developed several specialized physiological and biochemical mechanisms for acquiring and utilizing phosphorus. Our purpose here is to consider these mechanisms, especially as they relate to tropical forests. An emphasis is also placed on interactions between plant carbon supply and phosphorus acquisition. For more detailed recent reviews on plant P uptake, the reader is referred to Schachtman et al. (1998) and Raghothama (1999).

3.3.1 Distribution of Fine Roots and Mycorrhizal Associations

Generally speaking, most fine roots in tropical forest soils are found in the upper 0.5 m (Kerfoot, 1963), with a marked concentration of roots into a "root mat" close to the soil surface and within the litter layer being especially common on low-fertility soils (Stark and Jordan, 1978; Medina and Cuevas, 1989). It is generally considered that these root mats serve to ensure the maximum retention of nutrients by the vegetation and to minimize any leaching losses. Surveys of tropical forests have indicated almost ubiquitous mycorrhizal associations for such roots (Alexander, 1989; Janos, 1989).

As for temperate plants, it is widely assumed that mycorrhizal associations in tropical forests serve to improve the uptake of mineral nutrients, particularly phosphorus (Bolan, 1991; Koide, 1991; Smith and Read, 1997). Growth stimulations and enhanced P uptake in response to mycorrhizal infection have been reported for tropical tree seedlings (Janos, 1989; Lovelock et al., 1996, 1997).

Several mechanisms may be involved in enhanced P uptake by mycorrhizal symbioses. First, the extensive network of fungal hy-phae enables plants to explore a greater volume of soil, thereby overcoming limitations associated with the relatively slow diffusion of P in the soil solution (Marschner, 1995; Smith and Read, 1997). Second, although mycorrhizae often access phosphorus from the same labile pool as nonmycorrhizal roots, there is also some evidence that they are capable of accessing forms of phosphorus not generally available to the host plant (Marschner, 1995). Whether the mycorrhizae actually serve to increase the affinity of a root system for phosphorus or to allow plants to compete more effectively for phosphorus with soil microbes is unclear. For example, Thompson et al. (1990) reported that mycorrhizal roots and isolated hyphae have P uptake kinetics similar to those of nonmycorrhizal roots and other fungi.

This improved P uptake occurs in exchange for the provision of C from the host plant, and tire carbon requirements of tire mycorrhizal association can be substantial. For example, Baas et al. (1989) showed "root" respiration rates of mycorrhizal plant to be 20-30% higher than those of nonmycorrhizal plants. Similarly,

Jakobsen and Rosendahl (1990) observed 20% of plant carbon to be allocated below ground for nonmycorrhizal cucumber plants and 44% for those with mycorrhizal associations. In both cases, about half of this was respired. Working with subtropical Citrus species, Peng et al. (1993) suggested that root respiration rates were about 35% higher for mycorrhizal than for nonmycorrhizal roots.

The high carbon requirements of the mycorrhizal symbiosis have led to the suggestion that such symbioses may be enhanced when plant carbon supply is improved (Diaz, 1996). Nevertheless, as has been pointed out by Staddon and Fitter (1998), although increases in atmospheric [CO,] no doubt enhance (vesicular-arbuscular) mycorrhizal infection on a per plant per unit time basis, this may be a simple consequence of bigger plants at higher [C02]. That is, there may be no direct effect of carbohydrate supply on mycorrhizal colonization rates per unit root length once faster plant growth rates at elevated [C02] are taken into account (Staddon and Fitter, 1998).

Lovelock et al. (1996; 1997) investigated the interaction between myccorhizal infection and ambient [C02] in the shade-tolerant tropical tree Beilschmiedia pendula. They found mycorrhizal infection to stimulate growth and phosphorus uptake at both ambient and elevated [C02]. Mycorrhizal plants had similar, if not higher, tissue P concentrations at the higher [CO,]. This indicates an ability to maintain or perhaps even increase the degree of mycorrhizal infection per unit root length. This increased root system P uptake capacity seems to occur to nearly the same degree as the overall increase in plant growth. This is different from tire situation for nifrogen/C02 interactions, where tissue N concentrations nearly always decline with increasing [CO,] (Drake et al,

1997). Phosphorus uptake rates are therefore generally able to keep pace with metabolic requirements when growth is stimulated by increased [C02],

3.3.2 Organic Acid Exudation

It is now well documented that plant roots, bacteria, and fungi (including those involved in mycorrhizal associations) can all excrete organic acids into the soil solution (Marschner, 1995; Jones,

1998). As discussed in Sec. 2.3, some of these organic acids are capable of mobilizing sorbed P mainly by ligand exchange and occupation of P sorption sites (Lopez-Hernandez et al, 1986; Fox et al, 1990; Jones and Darrah, 1994; Bhatti et al, 1998). Consistent with this role for organic acids is the frequent observation that rates of organic acid exudation tend to increase in response to low levels of phosphorus availability (Jones, 1998). Although we know of no reports of organic acid exudation by plants native to moist tropical forests, there is no reason to suspect that this does not occur. In that context, the extent to which this organic efflux is modified by plant carbon supply is of relevance to the current analysis.

Changes in organic acid efflux at elevated [CO,] have been reported by Whipps (1985), Gifford et al (1996), DeLucia et al (1997), Barrett and Gifford (1999), and Watt and Evans (1999). On balance, these observations suggest that, when expressed per unit root length, there is little or no change in organic acid exudation rates (Watt and Evans, 1999). This situation is similar to the probable [C02]-independent plant-mycorrhizal infection rate when expressed per unit root length as discussed in Sec. 3.3.1. Similarly, this maintenance of the exudation rate per unit root length should allow plant phosphorus concentrations to be maintained at elevated [C02] (DeLucia et al., 1997; Barrett and Gifford, 1999).

3.3.3 Acid Phosphatase Exudation

As discussed in Sees. 2.1 and 2.3, soil phosphorus mineralization is governed by plant and microbial extracellular phosphatases which hydrolyze the ester bonds of organic P compounds. As for organic acid exudation, the extent to which plant extracellular phosphatases are active in improving the phosphorus nutrition of tropical forests is unknown. Nevertheless, we also note that, as for organic acids, the rate of root phosphatase activity increases with decreasing soil P availability (Barrett et al., 1998; Almeida et al., 1999), and rates of activity per unit root length are maintained under C.O, enrichment (Gifford el al, 1996; Barrett et ai, 1998) or nearly so (Almeida et al,, 1999). Thus, as for mycorrhizally mediated P uptake as well as P release mediated by organic acids, there is no reason to suspect that tropical forest phosphatase exudation rates per unit root length (or per unit root mass) should be reduced as CO, concentrations increase. To date there has been only one report of acid phosphatase activity for tropical forest soils (Olander and Vitousek, 2000). Working in Hawaii, they observed unusually high activities for this enzyme.

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