Transport of P in the fungus-plant interface

2.3.6.1 Transport of P in ECM

The transfer of P in mycorrhiza occurs either as: 1) passive translocation in the hyphae; or 2) passive and active transport of inorganic P into the root. Translocation of P within the hyphae occurs passively along a concentration gradient between the P source in the external hyphae and a P sink in the root supported by cytoplasmic streaming (Bolan, 1991). Transport in the hyphae is influenced by the intracellular P concentration of the hyphae because it regulates the P absorption by the fungus (Thomson et al., 1990;

Cairney and Smith, 1992). In addition, it has been proposed that motile tubular vacuoles may function in both intracellular and intercellular transport of mineral nutrients.

Pleiomorphic vacuolar tubules found in extraradical hyphae and in the fungal sheath containing polyphosphate move rapidly, extend, retract, fuse, and even pass through dolipore septa and are present throughout the entire fungal system (Orlovich and Ashford, 1994; Ashford, 1998; Shoji et al., 2006). These motile tubular vacuoles might be responsible for the rapid short and long distance transfer in the extraradical mycelium of ECM (Hyde and Ashford, 1997; Allaway and Ashford, 2001; Smith and Read, 2008).

A rapid bidirectional transfer of P and carbohydrates occurs between the root and the hyphae at the fungus-root interface (Figure 2.3-1). This involves both the passive efflux of P and carbohydrates through the fungal and plant plasma membranes into the interfacial apoplast and active exchange of nutrients between both partners (Smith and Gianinazzi-Pearson, 1988; Smith and Smith, 1989; Smith and Smith, 1990; Bücking and Heyser, 2000). For passive uptake into the plant, it is known that the contrast between the high P concentration in the hyphae of the Hartig net and the low P concentrations in the interfacial apoplast and the cortical cells causes the passive efflux of P from the hyphae into the interfacial apoplast and host plant (Smith et al., 1994). This occurs mainly by maintaining the P concentration gradient due to allocation of P either into P storage pools such as vacuoles in the cortical cells or to rapid transfer to P sinks such as the meristematic tissue and the nuclei of root cells (Bücking and Heyser, 1997) or aboveground plant parts. A second mechanism may also exist: high –low affinity P transporters have been identified which might be involved in the active transfer of P at the symbiotic interface (Smith and Read, 2008). This supply of P for plants might be quantitatively linked to loss of sugars to the interfacial apoplast. The relevance of both mechanisms and their dependence on ecological conditions is an area of further work particularly relevant to OM (see below). Also interesting would be stoichiometric approach

for the exchange between P and sugars, e.g. the mole sugars that are necessary for plant to deliver and to obtain one mole of phosphate.

2.3.6.2 Transport of P in AM

In arbuscular mycorrhizal associations P is transferred from the fungus to the plant and C from the plant to the fungus (Ezawa et al., 2002). The long distance transfer of P from the external mycelium to the plant is probably achieved via transfer of vacuolar components into the fungal arbuscules and from there to the interfacial apoplast (Ezawa et al., 2002).

The P-rich granules were shown to be the main form of P transport over long distances in AM fungi such as Glomus mosseae T.H. Nicolson & Gerd. (Callow et al., 1978; Cox et al., 1980). Ezawa et al. (2002) suggests that the transport would take place either by protoplasmic streaming or the motile tubular vacuole-like system. It is likely also that organic P molecules are present and may be part of the P pool delivered to the plant. A constant, length-specific P uptake by hyphae within AM species and a consequent P accumulation in AM hyphae were shown but exhibited a poor capacity for P delivery to the plant (Ezawa et al., 2002; Munkvold et al., 2004). Even if, as Harrison (1999) suggests, the presence of ATPases at the symbiotic interface indicates a possible active nutrient transfer, the biochemical and biophysical processes of this transfer across this interface is still unknown for AM.

2.3.6.3 Transport of P in OM

Fungi provide C, N and P to partially and fully mycoheterotrophic orchids (Figure 2.3-1).

However, little is known about plant-to-fungus transfer and subsequent benefits to the fungus (Cameron et al., 2006; Cameron et al., 2008). Cameron et al. (Cameron et al., 2006; Cameron et al., 2008) demonstrated a mutualistic, bidirectional C transfer between the green orchid Goodyera repens (L.) R. Br. and the fungus Ceratobasidium D.P. Rogers (Ceratobasidiaceae). After the initially mycoheterotrophic phase of development, the symbiosis in green-leaved adults follows the conventional pattern of mycorrhizal mutualisms: C from the plant is exchanged for mineral nutrients accumulated by the fungus (Cameron et al., 2007) (Table 2.3-3). Smith (1967) showed the direct transfer of

32P from fungus to protocorms and Alexander et al. (1984) the transfer of ³²P into Goodyera repens (L.) R. Br.. Cameron et al. (2007) showed for the first time that the intact external mycelium of Ceratobasidium cornigerum (Bourdot) D.P. Rogers (Ceratobasidiaceae) could assimilate P (supplied as ³³P) and facilitate its transfer to adult roots and shoots of G. repens (L.) (Table 2.3-3). This provides some evidence for reciprocal transfer of C and P in the Rhizoctonia-orchid symbiosis; the same has also

been shown to occur in the case of N (Cameron et al., 2006). Thus the mycorrhizas of Rhizoctonia-colonized orchids appear to function in the same way as those of AM and ECM systems. However, until now all knowledge is based upon the analysis of a single European orchid species. There is also circumstantial evidence that orchids may derive P from both, intact pelotons as well as lysed pelotons (Rasmussen and Rasmussen, 2009).

However, further work is required to delineate the exact means of P transport in orchids.

There is clearly a need to extend such analyses to regions with a far greater diversity of orchid species and with a wider range of nutritional and ecological gradients to deepen our understanding of the effect of environmental factors on physiological process like P transport.

Table 2.3-3: Phosphorus budget expressed as percentage of whole plant P