External hyphae of vesicular-arbuscular mycorrhizal fungi associated with Trifolium subterraneum L.
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1 New Phytol. (1992), 120, External hyphae of vesicular-arbuscular mycorrhizal fungi associated with Trifolium subterraneum L. 2. Hyphal transport of ^^p over defined distances BY I. JAKOBSEN\ L. K. ABBOTT^ AND A. D. ROBSON^ ^ Plant Biology Section, Environmental Science and Technology Department, Ris0 National Laboratory, DK-4000 Roskilde, Denmark ^ Soil Science and Plant Nutrition, School of Agriculture, The University of Western Australia, Nedlands, WA 6009, Australia {Received 26 July 1991; revised version received 5 December 1991) SUMMARY Phosphorus transport by hyphae of the three VA mycorrhizal fungi, Acaulospora laevis Gerdemann & Trappe, Glomus sp. and Scutellospora calospora (Nicol. & Gerd.) Walker & Sanders, associated with Trifolium subterraneum L. was investigated by means of radiotracer techniques. Plants with roots heavily colonized by each mycorrhizal fungus were transplanted to two-compartment systems, where a hyphal compartment was separated from the main compartment by a fine mesh preventing root penetration. The hyphal compartment contained layers of ^^Plabelled soil, which were placed at 0, 1, 2-5, 4-5 or 7 cm from the root compartment. A time-course study over 37 d showed that Glomus sp. transported most ^^P to shoots over soil^root distances shorter than 1 cm. In contrast, A. laevis transported most ^^P to shoots over soil-root distances longer than 1 cm. This ability of A. laevis to transport phosphorus over longer distances than Glomus sp. parallels previous observations that hyphae of A. laevis spread faster and further in soil than hyphae of the Glomus sp. Scutellospora calospora transported much less ^^P to plants, but accumulated more ^^P in its hyphae, than the two other fungi. The higher specific radioactivity in the hyphae of 5. calospora than of A. laevis and Glomus sp. indicated a retarded translocation of ^^P in its hyphae or retarded transfer of ^^P across its interface with the host. However, the poor phosphorus transport by S. calospora might also have resulted from its reaction to root trimming at transplanting; percentage root colonization by S. calospora decreased markedly after transplanting to the labelling system. Key words: Acaulospora laevis, external hyphae, Glomus sp., ^^P transport, Scutellospora calospora, time course study, Trifolium subterraneum. 1989). The importance of hyphal spread for the INTRODUCTION. rr i u u l *..u u * eiiectiveness or iungal phosphorus supply to the host The total length of external hyphae produced and therefore needs to be further investigated by direct the distribution of these hyphae in the soil may differ measurements of hyphal phosphorus transport by considerably between isolates of vesicular- different fungi. arbuscular (VA) mycorrhizal fungi (Abbott & ^^P has been used in studies with VA mycorrhizas Robson, 1985; Jakobsen, Abbott & Robson, 1991). to demonstrate directly hyphal phosphorus trans- In the study by Jakobsen et al. (1991), phosphorus port, which includes uptake, translocation and uptake by Trifolium subterraneum L. in association transfer across the symbiotic interface (Hattingh, with three different VA mycorrhizal fungi was Gray & Gerdemann, 1973 ; Pearson & Tinker, 1975 ; correlated with the spread of the external hyphae of Rhodes & Gerdemann, 1975; Cooper & Tinker, these fungi. However, the hyphal phosphorus trans- 1978, 1981). Each of these studies, however, included port from soil to host plant may also depend on only a single host-fungus combination which was differences in the proportion of hyphae, which are confined to culture systems of Petri dish size and metabolically active, and on differences in hyphal transport was studied over time intervals of only 10 d uptake and translocation capacities (Abbott & or shorter. Robson, 1984; Gianinazzi-Pearson & Gianinazzi, The objective of the present work was to compare
2 510 /. Jakobsen, L. K. Abbott and A. D. Robson the effectiveness of hyphae of three VA mycorrhizal fungi in their transport of '^P from the soil to their host plant, T. subterraneum. The symbioses were grown in a two-compartment system, similar in principle to that used by Jakobsen et al. (1991), but with a different design. ^^P was placed in the hyphal compartment at different distances from the roots and the time course of the appearance of ^^P in shoots of the host was measured. MATERIALS AND METHODS Species studied Hyphal transport of ^^P was studied in mycorrhizal associations between T. subterraneum cv. Seaton Park and Acaulospora laevis Gerdemann and Trappe [isolate WUM 11(4)], Glomus sp. [isolate WUM 10(1)] or Scutellospora calospora (Nicol. and Gerd.) Walker and Sanders [isolate WUM 12(2)]. The (a) 165 mm P solution r 1 i PVC tube 100/(m nylon mesh ' 50 mm Petri dish Figure 1. The two-compartment systems used for studying transport of ^^P by hyphae of VA mycorrhizal fungi in association with Trifolium subterraneum {a) and the modified Petri dish for the supply of ^^P to the hyphal compartment {b). E E o 00 Glomus isolate resembles Glomus fasciculatum (Thaxter) Gerdemann & Trappe emend. Walker and Koske. Plants receiving no inoculum were included as controls. Growth conditions The soil was a red earth sampled from a Karri {Eucalyptus diversicolor F. Muell.) forest at Lefroy Brook near Pemberton, Western Australia (McArthur & Clifton, 1975). This soil was selected because of its high phosphorus adsorption capacity. The soil was sieved through a 4 mm mesh and steamed for 1 h on two consecutive days. Nutrients were mixed in the soil at the following rates (mgkg-' dry soil): NH^NOg, 71; K^SO^, 152; 76; MgSO4.7H2O, 32; MnSO^.H^O, 16; ), 11; CUSO4.5H2O, 6; H3BO3, 1; ^ ), 0 35 and NaMoO4.2H2O, 018. A large phosphorus supply was needed to obtain acceptable growth rates of T. subterraneum in the red earth. Soil for the mycorrhizal treatments received 257 mg P kg-^ as KH2PO4, an amount which will support 70 % of maximum growth of nonmycorrhizal T. subterraneum in the red earth (unpublished results). Soil for the non-mycorrhizal controls received twice as much phosphorus in an attempt to obtain similar grow^th rates of mycorrhizal and non-mycorrhizal plants. Crude soil inoculum of the three VA mycorrhizal fungi was mixed into the soil to obtain spore densities similar to those used by Jakobsen et al. (1991). Lots of 260 g of these soil mixes were filled into PVC tubes (diameter = 60 mm) placed in 1'5 kg pots with steamed soil packed around them. The downward opening of the tubes bad been cut at a 45 angle. The soil inside and outside tubes was watered to 65 % of field capacity and left to incubate in a glasshouse, where day/night temperatures were maintained at 20/15 C. One week later three germinated seeds of T. subterraneum were sown in each tube. Facb seed received 0"5 ml of a dense suspension of Rhizobium leguminosarum biovar trifolii (TAl) in 1 % sucrose. After emergence, seedlings were tbinned to one per tube and the soil surface was covered with alkathene beads. Twenty plants were prepared for each of the three mycorrhizal treatments, while ten non-inoculated control plants were included. Plants were transferred to the ^^P-labelling units 32 d after planting, when mycorrhizal colonization had become well established in all inoculation treatments. These units were PVC boxes (H x L x W = 180 X 160 X 100 mm) which were divided in two compartments by a PVC plate holding the hyphal compartment; the plate was inserted at a 45 C angle and hyphal and root compartments were separated by a 37 //m mesh (Fig. 1 a). Fifteen uniformly sized plants were selected from each inoculation treatment in addition to six plants from the control treatment.
3 External hyphae of mycorrhizal Trifolium subterraneum 511 Before transfer of plants, roots growing out from the bottom of the PVC tubes were excised along the 45 C cut. The exposed soil surface with roots and hyphae was placed 5 mm from, but adjacent to, the mesh dividing the root and the hyphal compartments, and 1150 g dry soil was packed around each PVC tube. Pots were returned to the controlled-temperature greenhouse and soil moisture was maintained at 65 % field capacity by daily watering. Symptoms of nitrogen deficiency appeared 4 5 d later and 25 mg N as NH4NO3 was supplied to each pot. Preparation of hyphal compartments with ^^Plabelled soil ^^P was supplied to 15 g soil lots held between discs of 100/im nylon mesh in Petri dishes (50 mm diameter), where large holes (40 mm diameter) had been cut in both the lid and bottom (Eig. 16). Three ml carrier-free radioactive orthophosphate in aqueous solution (616-7 kbq ml"^) were pipetted onto the soil surface at one side of each Petri dish and allowed to dry. The ^^P dish was placed inside the hyphal compartment at 0, 1, 2-5, 4-5 or 7 cm from the root compartment with the labelled soil surface facing the roots. The hyphal compartments were made from perspex tubing (50 mm diameter, 80 mm length) and contained 190 g dry soil, including the soil in the ^^P dishes. The soil had been sieved through a 2 mm mesh and mixed with nutrients at the same concentrations as soil in the root compartments. The distal end of the hyphal compartments was closed by a 100 fim nylon mesh. Three replicate compartments were prepared for each combination of inoculation treatment and distance of ^^P placement. Only the 0 and 1 cm distances were included for the non-mycorrhizal treatment and the labelling experiment involved 51 pots in total. Harvest and measurements The time-course of transport of ^^P into the shoots was monitored on leafiets harvested from each plant every third day after transfer of the plants to the ^^P units. One leafiet was sampled from each of the second-youngest fully expanded trifoliate leaves of 4-6 shoot apices of each plant. The fresh leafiets from each plant were placed fiat inside an inverted plastic screw cap (35 mm diameter) which fitted on to a scintillation probe for beta-radiation (Nuclear Chicago) and enabled the leafiets to be firmly held against the scintillation window during two 60 s counting periods; all counts were corrected for isotope decay. A similar method was used by Jupp, Newman & Ritz (1987) for monitoring radioactivity in undetached leaves of Lolium perenne. Total uptake of ^^P in plants was measured after 37 d when all plants were harvested. Roots adjacent to the hyphal compartment and subsamples from inside and outside the PVC tube were retained for measurements of mycorrhizal colonization and root length (Jakobsen et al, 1991). All other plant material was dried at 70 C, weighed and analyzed for total phosphorus content by the molybdovanadophosphate method (Boltz & Lueck, 1958) after acid digestion (Johnson & Ulrich, 1959). Radioactivity in the digests was measured by Cerenkov counting (Kessler, 1986) on a Packard 1500 scintillation analyser; results were corrected for counting eflficiency and isotope decay. The soil from the hyphal compartments of the 70 mm treatments was pushed out of the perspex tubes and transverse sections of the soil columns were made at 10, 20, 30, 40, 50 and 70 mm distance from their proximal end. Soil columns from the 0 mm non-mycorrhizal treatments were sliced at 10, 20 and 30 mm from the bottom of the *T vial. The length of hyphae in these soil sections was measured as described by Jakobsen et al. (1991) except that 1 instead of 5 ml aliquots were pipetted onto the membrane filters. Hyphae were also washed from the 0-25 mm sections from two replicates of each treatment by repeated aqueous suspension and decanting onto a 250/^m sieve. The radioactivity of the collected hyphae was measured after acid digestion as for the analysis of plant material. RESULTS Plant growth and mycorrhizal formation Dry matter production, phosphorus content and root length at time of transplanting to the ^^P system were less for the inoculated treatments than for the control plants, which had received additional phosphorus (Table 1, ^ = 0 d). When plants were harvested from the ^^P-labelling units 37 d later, the uninoculated controls were still the largest, while dry weights, phosphorus contents and root lengths now differed between inoculation treatments (Table 1, I = 37 d). Dry weight and phosphorus content in shoots decreased in the order Glomus sp., A. laevis, S. calospora; in contrast, dry weight and length of roots were higher with S. calospora than with the two other symbioses. Plant growth within each inoculation treatment was unaffected by the distance of '^^P placement. Phosphorus concentration of the leafiets was rather similar and changed only little with time in the non-mycorrhizal controls and in the symbioses with A. laevis and Glomus sp.; in contrast, phosphorus concentration in leafiets of T. subterraneum associated with S. calospora decreased markedly during the first 9 d after transplanting to the ^'T system (Table 2). About 80 % of the root length had been colonized by the mycorrhizal fungi in all three inoculation treatments at the time of transplanting (Table 1, i = 0 d); 37 d later the percentage colonization of roots adjacent to the 37 //m mesh was even higher with
4 512 /. Jakobsen, L. K. Abbott and A. D. Robson Table 1. Dry weight {D. tvt), phosphorus content (P), root length {RL) and percentage of root length colonized in Trifolium subterraneum associated or not {control) with three VA mycorrhizal fungi Fungus and harvest D. wt (g f)ot ^) Shoot Root P (mg pot -1) Shoot Root RT (m pot"^) zation (%) Harvest 1 (/ = 0 d) Acaulospora laevis Glomus sp. Scutellospora calospora Control 0-20 b 0-16 b 0-21 b 0-28 a 0-86 b 0-75 b 0-83 b l-12a ll-6b ll-6b 10-5b 18-la 78 a* 83 a 81a Ob Harvest 2 (< = 37 d) A. laevis Glomus sp. S. calospora Control 3-69c 4-33 b 2-51 d 5-22a l-71c l-79c 2-25 b 3-22a 12-OOb 15-84a 5-03 c 15-32a 6-50a 6-48 a 2-95 c 5-65 b 216b 232b 336a 90 at 97 a 47 b Oc, not determined. Means with the same letter within one harvest are not significantly different (P > 0-05, Duncan's New Multiple Range Test). Measured on root sample from PVC tube. t Measured on roots adjacent to mesh separating the root compartment and the hyphal compartment. Table 2. Phosphorus concentration (% of D. wt) in leaflets sampled from Trifolium subterraneum associated or not {control) with three VA mycorrhizal fungi Days after transfer to'': P system Fungus Acaulospora laevis Glomus sp. Scutellospora calospora Control 0-42* * Leaflets from replicate pots pooled before analysis. Glomus sp. and A. laevis, whereas, with S. calospora, it had decreased to only 47% (Table 1). Roots sampled from outside the PVC tube were less colonized, especially with S. calospora (5 %), but also with A. laevis (67%) and Glomus sp. (59%). All uninoculated plants remained non-mycorrhizal throughout the experiment. Hyphae of all three inoculant fungi had grown into the hyphal compartment after 37 d (Fig. 2) and spores had been formed by A. laevis and 5'. calospora. The length of hyphae per gram dry soil was not significantly affected by the fungal treatments for the segments 0-1, 1-2 and 2-3 cm from the root compartment. High hyphal densities were maintained in the 5-7 cm segments by A. laevis and Glomus sp., whereas the hyphal length of S. calospora decreased to the background levels over the 5-7 cm interval (Fig. 2). The time-course of hyphal uptake of ^^P High levels of radioactivity were measured with the scintillation probe on intact leaflets in the symbioses with Glomus sp. and A. laevis, whereas activity was low in leaflets from plants colonized by S. calospora (Fig. 3). Radioactivity was detected for the first time after 9 d in plants colonized by Glomus sp. and A. laevis and with the '*^P adjacent to the root compartment {d = 0 cm) (Fig. 3 a). Radioactivity in leaflets from these treatments increased with time, reached a maximum plateau after d and then decreased. During the d period higher levels of radioactivity were measured in leaflets of the symbiosis with Glomus sp. than with A. laevis. The much lower levels present in the S. calospora symbiosis increased slowly with time while the radioactivity in the nonmycorrhizal controls remained at a constant low level throughout the period of measurement (Fig. 3 a). The uptake of *'^P placed 10 mm from the root compartment was delayed by 3-4 d as compared to the 0 cm treatment (Fig. 36). Levels of radioactivity were very similar in leaflets from the Glomus sp. and the A. laevis symbioses throughout the period of measurement. The pattern of an initial increase, a
5 External hyphae of mycorrhizal Trifolium subterraneum Distance from root compartment (cm) o Figure 2. Length of hyphae in soil sections from the X hyphal compartment of the experimental units with Trifolium subterraneum in association with Acaulosporas laevis ( ), Glomus sp. (G) or Scutellospora calospora (H). Values were corrected for background hyphae (8'5 m g~' dry soil) measured in hyphal compartments from nonmycorrhizal plants. Bars represent 1 SEM. D) E Q. O peak and a decrease was similar to that observed in tbe 0 cm treatment. Radioactivity in leafiets of tbe 5'. calospora symbiosis could not be detected until after 27 d and the control plants contained only traces of radioactivity after 37 d (Fig. 36). The appearance of radioactivity in the leaflets was further delayed when tbe ^^P was placed 25 mm from tbe root compartment, but could now be detected earlier in tbe A. laevis than in the Glomus sp. symbiosis (Fig. 3 c). Furthermore activities in leaflets of the A. laevis symbiosis reached the same levels as in the 1 cm treatment (Fig. 36), whereas radioactivity in tbe Glomus sp. symbiosis was now reduced by more than 50%. A plateau was reached in botb symbioses after 30 d. Traces of ^^P were detected witb S. calospora. Tbe difference between tbe A. laevis and the Glomus sp. symbioses was even more pronounced in the 4-5 cm treatment, although the maximum levels observed witb A. laevis were decreased to one third of the levels recorded in the 2-5 cm treatment (Fig. Zd). When the '^^P was placed 7 cm from the roots radioactivity was detected only in the A. laevis symbiosis after 37 d (data not presented). Total content of '^P in plants and external hyphae Measurements of total radioactivity in plants after 37 d were in accordance with the time-course observations. Hypbae of Glomus sp. bad transported more ^^P to tbe host plant than hyphae of A. laevis, when the ^^P was placed 0 and 1 cm from the root compartment; in contrast transport was highest with A. laevis at further distances of placement (Fig. 4). Taken over the 0-7 cm interval hyphal transport of ^^P to the plant was higher with A. laevis than with o '-a ro DC 20 Time (days) Figure 3. The time-course of appearance of radioactivity in young leaflets of Trifolium subterraneum in association with Acaulospora laevis (%), Glomus sp. ( ), Scutellospora calospora (V) or left non-mycorrhizal ( x ). Distances (cm) between the ''-P-labelled soil and the root compartment were 0 (a), 1 (b), 2-5 (c) or 4-5 (d). Bars represent SEM. Glomus sp. The total radioactivity measured in plants colonized by Glomus sp. and A. laevis and with the ^"^P placed adjacent to the roots (0 mm) corresponded to 8-4 and 6-0 %, respectively, of the total amount of *^P applied to the soil. A significant *^P transport by byphae of 5. calospora occurred only from the 0 and 1 cm placements and levels of radioactivity reached only about 10% of tbose obtained witb tbe other two fungi. Non-mycorrhizal control plants absorbed small but significant amounts of ^^P from tbe 0 cm placement, wbereas only traces of ^^P were absorbed
6 514 I. Jakobsen, L. K. Abbott and A. D. Robson ^^P placement (cm from roots) Figure 4. Total transport of ^^P into Trifolium subterraneum (shoot-i-root) in association with Acaulospora laevis (#), Glomus sp. ( ), Scutellospora calospora (V) or left non-mycorrhizal (x ). Plants were harvested 37 d after transplanting to the system with ^^P-labelled soil placed in the hyphal compartment at five distances from the root compartment. Bars represent SEM. Table 3. Dry weight and radioactivity of hyphae washed from the cm soil section of the hyphal compartments of two replicate pots of each treatment Fungus Acaulospora laevis Glomus sp. Scutellospora calospora Control, not determined. Dry weight (mg) '''P activity (dpm mg"^ D.wt X 10"^) from the 1 cm placement. This confirms that diffusion of phosphorus was very slow in this soil with high sorption capacity. The dry weight of external hyphae in the cm soil column of the hyphal compartment was similar for all fungal species in each of two sets of replicate pots (Table 3). In contrast the specific radioactivity in external hyphae of 5. calospora was up to four times as high as the activity in hyphae of the two other symbioses (Table 3). The radioactivity in the hyphae of 5. calospora corresponds to 85 "o of the total *'^P absorbed from the 2-5 cm placement. The corresponding figures for Glomus sp. and A. laevis were only 3 and 1 "o, respectively. DISCUSSION The first paper of this series described how the spread of external hyphae differed considerably between the three VA mycorrhizal fungi and the results indicated a relationship between phosphorus uptake and hyphal spread (Jakobsen et al., 1991). The direct measurements of hyphal phosphorus transport, reported in the present paper, confirm these relationships for Glomus sp. and A. laevis, while hyphae of S. calospora transported only little phosphorus from the soil to the host. In previous studies of phosphorus transport by hyphae of VA mycorrhizal fungi using *^P techniques, the isotope was not supplied until hyphae had become well established in the hyphal compartment 6-10 wk after planting (Hattingh et al., 1973 ; Rhodes & Gerdemann, 1975 ; Cooper & Tinker, 1978, 1981). Our experimental system included five fixed distances between the plant roots and the *^P, which was already present when hyphae were allowed to grow into the hyphal compartment. The design was crucial for the accomplishment of this first time-course study of hyphal phosphorus transport across distances from 0 to 7 cm. The lag of 6-9 d before *'^P appeared in the shoots was longer than the 3 d lag period observed by Cooper & Tinker (1978, 1981), but in the present work hyphae would have to pass through a soil layer of c. 5 mm thickness before reaching the *^P-labelled soil placed adjacent to the root compartment (0 cm treatment). The transient higher specific radioactivity (cpm g"^ D. wt) measured in the Glomus sp., than in the A. laevis-colonized plants of the 0 mm treatment, was not related to the hyphal densities in the 0-1 cm soil layer, which at 37 d tended to be highest in the A. laevis treatments. This indicates that the capacity for phosphorus transport was higher in hyphae of Glomus sp. than of A. laevis. Another possibility is that initiation of hyphal growth occurred sooner with Glomus sp. than with A. laevis as, in a previous experiment, hyphal densities at 1 cm distance from the roots of 14- and 28-d-old plants were actually higher with Glomus sp. than with A. laevis (Jakobsen et al., 1991). However, the faster spread of hyphae of ^. laevis demonstrated by Jakobsen et al. (1991) enables this fungus to transport most phosphorus from beyond 1 cm distance and from the hyphal compartment in total (Figs 3, 4). The decrease with time in specific radioactivity of leaflets subsequent to a maximum plateau or peak possibly reflected a reduced ability of older hyphae to absorb phosphorus. Accordingly, Rhodes & Gerdemann (1975) applied *^P at 1 cm intervals to a hyphal compartment with an established mycelium of G. fasciculatum and found the hyphal transport of *'^P to the plant to be four times as high from the 3 and 4 cm distances as from the 1 and 2 cm distances of application. Biochemical studies have also shown that the metabolic activity of hyphae of VA mycorrhizal fungi change with time (Schubert et al., 1987; Sylvia, 1988). The superior ability of A. laevis hyphae to transport phosphorus from a hyphal compartment to the host plant in a previous experiment (Jakobsen et
7 External hyphae of mycorrhizal Trifolium subterraneum 515 al, 1991) was reflected in higher dry weights of A. laevis colonized plants than of plants colonized by Glomus sp. In that experiment the major phosphorus supply to the plants occurred from the larger hyphal compartment. The root compartment was larger than the hyphal compartment and thus the phosphorus source for the plants in the present experiment. Plants grew better in this experiment with Glomus sp. than with A. laevis. Hyphal spread would have been less important in this case with average root densities of cm cm~^. The higher phosphorus uptake of plants colonized by Glomus sp. than of plants colonized by A. laevis is in agreement with the observed differences in hyphal uptake of ^^P placed close to the roots. Hyphae of S. calospora were present in the 0-3 cm interval of the hyphal compartment in amounts similar to those found for the two other fungi. However, the transport of ^^P to the plant by hyphae of S. calospora was only small and accordingly the phosphorus uptake and growth of plants colonized by S. calospora was much smaller during the radiolabelling period than phosphorus uptake and growth of the two other symbioses. The surprisingly high specific radioactivity of 5. calospora hyphae in comparison to hyphae of the two other fungi might lead to the conclusion that hyphal phosphorus transport from soil to host plant was limited more by processes involved in hyphal translocation and transfer across the host-fungus interface than by hyphal phosphorus uptake per se. This is in accordance with higher root-shoot ratios of radioactivity with 5. calospora ( as a mean of the 0, 1 and 2-5 cm treatments) than with Glomus sp. and A. laevis (corresponding figures were and , respectively). However, the poor performance of S. calospora after transplanting to the ^^P-labelling system is in contrast to its performance during the pre-transplanting period and in a previous experiment (Jakobsen et al, 1991). Percentage colonization inside the PVC tube decreased considerably after transplanting and roots growing out from the bottom of the PVC tube became only sparsely colonized. Consequently, it appears that growth and general physiological performance of S. calospora reacted drastically to the trimming of roots at transplanting as compared to the two other fungi tested. Perhaps the maintenance of functional integrity after disturbance of a VA mycorrhizal fungus is somehow related to the presence of vesicles in the roots; such vesicles, believed to have a storage function, are absent from roots colonized by S. calospora. In conclusion, it seems likely that the observed low uptake of ^^P by hyphae of 5. calospora may not be an inherent feature of that fungus but rather a reaction to disturbance of the symbiotic system. Further comparative work involving different degrees of disturbance is needed to test this hypothesis. Autoradiographic studies of mycorrhizal effects on phosphorus depletion around roots led Owusu- Bennoah & Wild (1979) to the conclusion that mycorrhizas improved phosphorus uptake by increasing the depletion zone by about 1 mm. This was in major contrast to Rhodes & Gerdemann (1975), who found hyphal transport of ''^P to occur over at least 7 cm distance. Their findings are confirmed by the present work, which clearly shows that hyphal phosphorus transport over several cm distance is quantitatively just as important as hyphal phosphorus uptake close to the roots. Presumably the narrow growth containers used by Owusu-Bennoah & Wild (1979) were somehow inhibitory to hyphal spread. Hyphae of VA mycorrhizal fungi clearly have a potential for transport of phosphorus over larger distances than demonstrated by Rhodes & Gerdemann (1975) and by the present study as hyphae of A. laevis can spread 11 cm or more in 47 d (Jakobsen et al, 1991). The present work confirms the usefulness of radioisotopes in studies of nutrient transport by fungal hyphae. The placement of ^^P at defined distances from the roots in combination with a timecourse study, provided information on the hyphal spread, on the ability of hyphae to maintain phosphorus uptake from a certain site in the soil and on the ability of the hyphae to transport phosphorus over different distances. The experimental system used appears to be generally useful for characterizing growth patterns and nutrient uptake characteristics of external hyphae of VA mycorrhizas as influenced by fungus, host and soil. ACKNOWLEDGEMENTS This work was carried out at UWA while LJ. held a position as a Visiting Research Fellow funded by the Danish Agricultural and Veterinary Research Council. We wish to thank Christina Blackburn, Chris Gazey and David Jasper for assistance and support throughout the study. REFERENCES ABBOTT, L. K. & ROBSON, A. D. (1984). The effect of mycorrhizae on plant growth. In: VA Mycorrhiza (Ed. by C. LI. Powell & D. J. Bagyaraj), pp CRC Press, Boca Raton, Florida. ABBOTT, L. K. & ROBSON, A. D. (1985). Formation of external hyphae in soil by four species of vesicular-arbuscular mycorrhizal fungi. New Phytologist 99, BOLTZ, D.F. & LUECK, C. H. (1958). Phosphorus. In: Colorimetric Determination of Non-Metals (Ed. by D. F. Boltz), pp Interscience Publishers, New York. COOPER, K. M. & TINKER, P. B. (1978). Translocation and transfer of nutrients in vesicular arbuscular mycorrhizas. II. Uptake and translocation of phosphorus, zinc and sulphur. New Phytologist 81, COOPER, K. M. & TINKER, P. B. (1981). Translocation and transfer of nutrients in vesicular-arbuscular niycorrhizas. IV. Effect of environmental variables on movement of phosphorus. New Phytologist 88, GIANINAZZI-PEARSON, V. & GIANIN.AZZI, S. (1989). Phosphorus
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