PLANT GROWTH RESPONSES TO VESICULAR-ARBUSCULAR MYCORRHIZA
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1 New Phytol. (72) 71, PLANT GROWTH RESPONSES TO VESICULAR-ARBUSCULAR MYCORRHIZA III. INCREASED UPTAKE OF LABILE P FROM SOIL BY D. S. HAYMAN AND B. MOSSE Rothamsted Experimental Station, Harpenden, Hertfordshire {Received May 71) SUMMARY Onion plants were grown in a range of soils labelled with '^P. It was found that although the mycorrhizal plants had taken up more phosphorus and grown larger, the proportion of ^^P to total P (specific activity) taken up by mycorrhizal and nonmycorrhizal plants after 10 weeks was not significantly different. It is concluded that the mycorrhizal roots used the same source of labile phosphate but explored a greater volume of soil beyond the zone of phosphate depletion near the root surface. There was no indication that mycorrhizal roots had access to sources of phosphate different from those accessible to nonmycorrhizal roots. The specific activity of NaHCOj-extractable phosphorus differed considerably between the eight soils but the specific activity of absorbed phosphorus in the plants always corresponded closely to that of the soil in which they had grown. INTRODUCTION In phosphate-deficient soils plants infected with vesicular-arbuscular (VA) mycorrhiza usually take up more phosphorus and grow better than nonmycorrhizal plants (Baylis, 67; Gerdemann, 68; Hayman and Mosse, 71; Nicolson, 67). How the mycorrhizal plants obtain the extra phosphorus is not clear. Although VA mycorrhizal roots take up more phosphorus from solution than nonmycorrhizal roots (Bowen and Theodorou, 67; Gray and Gerdemann, 69), the same mechanism does not necessarily account for their greater uptake of phosphorus from the soil because the major factor normally limiting uptake in soil is the number of phosphate ions at the root surface (Sutton and Gunary, 69). Two possible mechanisms are: (i) hyphae of mycorrhizal roots can absorb phosphate from insoluble forms not available to nonmycorrhizal roots; and (2) hyphae extend into the soil and absorb soluble phosphate beyond the phosphatedepleted zone close to the root surface. The first possibility can be tested by labelling soil with ^^P and comparing the specific activities of the phosphate absorbed by mycorrhizal and nonmycorrhizal plants growing in it. In a short experimental period organic and insoluble phosphates in soil will not become labelled to any appreciable extent. Therefore, if mycorrlaizal plants can utilize these sources of phosphate while nonmycorrhizal plants cannot, the specific activity of absorbed phosphate in the mycorrhizal plants will be lower. MATERIALS AND METHODS Soils The eight soils used were from cultivated land (nos. 7 and 12), grassy common (i^o- 11), deciduous forest (no. 8) and heath (nos. 10, 15, 16 and ) (Hayman and Mosse, 41
2 42 D. S. HAYMAN AND B. MOSSE 71). They were sieved, mixed with peat in proportions of 3 parts soil to i part peat (by volume) and irradiated with a gamma dose of 0.8 Mrad. One quarter (by weight) sterilized sand was mixed with each soil, and lime was added to raise the ph to 6.5. Soluble phosphorus was estimated in 0.5 M NaHCOj at ph 8.5 and in o.oi M CaClj. Table i shows the phosphate contents of the eight soils. They were from the same sites as used in earlier experiments (Hayman and Mosse, 71), but the amounts of available phosphate and the plant growth responses were different in some of the soils. Table i. Phosphorus contents of the eight experimental soils Amounts of soil phosphorus mg total mg/iooo g soil //moles/i P/1000 g Soil no. 7 (F) 8 (F) IO (O) II (F) 12 (O) 15 (O) 16 (O) (O) ilf soluble in NaHCO 3 soluble in CaCl S-4 3-2O (4.6)* 0.97 (47.2)* * Solution too coloured for reliable Olsen test. t Determined colorimetrically with molybdenum blue after fusion with sodium carbonate. (F), Fresh collection from same site as before (Hayman and Mosse, 71): (O), original soil sample stored moist for about 2 years. A solution containing ^^P (2/^Ci//jg P) was added to the test soils at the rate of ioo /xci/kg soil. After standing 2 days each soil was thoroughly mixed with a Kenwood mixer, moistened to field capacity and kept moist. Specific activities were measured weekly in samples extracted in 0.5 M NaHCOj, and equilibrium between labile P and added ^^P was considered to have been reached after 3I weeks (Table 2). The figures in column tp represent the theoretical dilution of '^^P immediately after application to the soil; they are calculated by dividing the activity of ^^P added, by the mean of the NaHCOjextractable P determined on days ii, i8 and 25. Figures in the last column (tgo) represent the calculated specific activity on day 80, when specific activity of the plant phosphorus was determined. The soils were distributed into pots and planted 4 weeks after addition of the ^^P. Plants Onion seedlings, Allium cepa var. James' Long Keeping, were grown in 3-in. pots, two per pot and three replicate pots, and watered and fed as before (Hayman and Mosse, il no II 12 IS 16 Table 2. Rate of equilibration of soil P with P in the eight soils cpm 1 figp soluble in NaHCO 3 (specific activity) to* After 11 days After 18 days After 25 days I3II tsot S 12.7 * to = theoretical specific activity at zero time. t t8o = calculated specific activity on day 80 when specific activity of plant phosphorus was measured. Figures in the first four columns have been adjusted for decay and are directly comparable.
3 uptake of labile P from soil 43 71). They grew for 4 weeks in a glasshouse with supplementary lighting, then 6 weeks in a Saxcil growth cabinet with 16 hours light (24,000 lx) at 21 C and 8 hours dark at 16 C, and a relative humidity of 70%. Treatments Seedlings germinated in sterilized sand were planted in two sets of irradiated no. 8 soil. One set was made mycorrhizal by inoculating with Endogone (yellow vacuolate spore type, Mosse and Bowen, 68), the inoeulum of sporocarps, mycelium and infected root pieces being placed in each planting hole. The other set (eontrols) was given sporocarp teachings containing the micro-organisms that contaminated the sporocarps. When transplanted after 3 weeks to the test soils, the mycorrhizal seedlings weighed an average of 10.3 mg and contained mg P, and the nonmycorrhizal seedlings weighed an average of io.o mg and contained S P- Measurements Fresh and dry weights of shoots and roots were measured at the end of the experiment. The phosphorus contents of washed shoots and roots, ground up and ashed with magnesium aeetate at 450 C and dissolved in HCl, were determined colorimetrieally by the molybdenum blue method using a Technicon auto-analyser. The amount of ^^P present in the washed shoots and roots was determined on either 50- or ioo-mg ground samples on aluminium planchets in a i-in. Geiger-Muller counter with an automatic sample changer and counted for either 1000 or 5000 seconds. The analyses of total P and ^^P were done on samples derived from the two seedlings from each pot combined. Where the combined dry weights were less than 50 mg, the whole sample was placed on the planehet and counted. RESULTS After 18 days equilibration the specific activity of NaHCOj-extractable phosphorus in the soil changed little (Table 2). After 25 days equilibration it ranged from 120 cpm/ /'g P for soil 16, with most extractable phosphorus, to 1404 cpm//jg P for soil 15 with least. In general the measured specific activity on day 11 (Table 2, column 2), was related to the calculated theoretical specific activity at zero time (Table 2, column to), which is ti measure of the expected specific activity on the basis of dilution with the NaHCOjt'Xtractable phosphate. The ratio to/specific activity on day 11 is not, however, the same for all the soils, indicating that other factors, perhaps exchange with other kinds of labile phosphate, affect the specific activity. In all eight soils the specific activity of absorbed phosphorus in the mycorrhizal plants Was very similar to that in nonmycorrhizal ones (Table 3). The differences were not significant at P = Therefore, under our experimental conditions, mycorrhizal and nonmycorrhizal plants had taken up similar amounts of ^^P per unit total phosphorus. 'Similar results were also obtained in a preliminary experiment with two soils (nos. 8 and 'i)- For all soils the specific activity of phosphorus absorbed by plants (Table 3) was similar to that of NaHC03-extractable soil phosphorus adjusted for decay (Table 2, column tgo). Except for soil the activity of the soil phosphorus was always slightly greater. This could be due to a continued slow equilibration of the ^'^P in the soil. In all eight soils the mycorrhizal plants took up more phosphorus (Table 4) and grew
4 44 D. S. HAYMAN AND B. MOSSE Table 3. Specific activities ofphosphorus absorbed by mycorrhizal and nonmycorrhizal onions grown in eight soils {mean of three replicates) il no II cpm//ig P taken up Mycorrhizal plants Nonmycorrhizal plants Shoots Roots II.I Roots Shoots * * Negligible uptake of P. bigger (Table 5) than the nonmycorrhizal ones. Although the mycorrhizal roots weighed more and, therefore, were probably more extensive and explored more soil, the root/ shoot ratios of mycorrhizal plants were generally smaller (Table 5) than those of nonmycorrhizal plants in the same soil. In a previous experiment this was even more marked (Hayman and Mosse, 71). In the present experiment (Table 5) root/shoot ratios were very similar in soils 8 and 12; in soil that of mycorrhizal plants was even slightly Table 4. Phosphorus content of mycorrhizal and nonmycorrhizal onions grown in eight soils {mean ofsixplants) Total phosphorus/plant (mg) Mycorrhizal plants Nonmycorrhizal plants Soil no. Shoots Roots Shoots Roots II s larger, but nonmycorrhizal plants in this soil were so small that a small loss of plant material during harvesting would greatly distort the figures. As VA mycorrhiza causes little change in root morphology it is clear that per unit shoot weight the absorbing surface of mycorrhizal roots is the same or smaller than that of nonmycorrhizal roots. Hence, since mycorrhizal plants have taken up more phosphorus (Table 4), their roots must be more efficient in uptake Table 5. Dry weights and root I shoot ratios of mycorrhizal and nonmycorrhizal onions grown in the eight soils {mean of six plants) Dry weight/plant (mg) Mycorrhizal plants Nonmycorrhizal plants ii no II Shoots Roots ~ Root/shoot ' Shoots " K001 ~ Root/shoot ratio ratio s S 0.83
5 uptake of labile P from soil 45 DISCUSSION These results show that, although mycorrhizal plants clearly took up more phosphate from the soil than nonmycorrhizal ones (Table 4), the specific activity of the absorbed phosphorus was very similar in both (Table 3), indicating that they had used the same, or similarly labelled, sources of phosphate. Similar results have recently been obtained by Sanders and Tinker (71). The correspondence, in all eight soils, between specific activities of absorbed phosphorus in the plants and the NaHCOj-extractable phosphorus in the soil further suggests that the latter was the chief source of phosphorus for both mycorrhizal and nonmycorrhizal plants. These results were unexpected, because Daft and Nicolson (66) and Murdoch, Jackobs and Gerdemann (67) showed that VA mycorrhiza improved growth of plants in sand when the only source of phosphate was 'unavailable', e.g. rock phosphate or apatite, and this has generally been taken as evidence that VA mycorrhiza hydrolysed insoluble phosphates. If this were so the specific activity of their absorbed phosphorus in our experiment should have been lower. A possible explanation of the improved growth of mycorrhizal plants given insoluble phosphate is that mycorrhizal roots, by virtue of their external hyphae, may have a greater area of close contact with surfaces where phosphate ions are dissociating chemically. Small amounts of phosphate will dissociate from rock phosphate to form an equilibrium with the soil solution. If these ions are taken up more efficiently by the external hyphae, more ions will dissociate chemically to restore the equilibrium. With ectotrophic mycorrhiza also there has been uncertainty about the source of the additional phosphate taken up by the mycorrhizal plants. Hydrolysis of insoluble inorganic phosphates, of organic phosphates (phytates) and extra absorbing surface of the branched roots have been considered the most likely explanations. The experimental evidenee has been reviewed by Harley (69). Although the metabolism of mycorrhizal roots differs from that of uninfected roots in several respects (increased respiration rates and sugar levels have been recorded), this may not be a relevant consideration. The uptake of phosphate, especially from low phosphate soils, is thought to be controlled by slow rates of movement of these ions in the soil, so that the limiting factor is not the ability of the root to take them up, hut the ability of the phosphate ions to reach the absorbing surface. Changes in absorbing surface area are therefore more likely to affect uptake than changes in metabolism. Unlike the ectotrophic mycorrhiza, VA mycorrhiza causes little change in root morphology, but could greatly increase the volume of soil explored if the external hyphae acted as additional absorbing surface. Hyphae, by virtue 01 their very large surface per unit weight, could be a very efficient uptake system. In addition mycelium of Endogone has the unusual characteristic that growth is not restricted *-o the hyphal tip, but fine, thin-walled, much branched, rhizoid-iike hyphae can arise laterally from fully mature, even very old thick-walled main hyphae. Also the fungus, being a phycomycete, has few septa and the nnigration of cytoplasm from hyphae that h'ive apparently become functionless to other growing parts of the hyphal system may be observed. The empty part is then cut off by a septum. The extent of the external mycelium ifi the soil and the number and viability of hyphal links between it and the mycelium in tile roots may vary with the soil. Nicolson (60) noted that the external mycelium was much better developed in the fixed yellow zone than in other zones of sand dunes, and ^e noticed (Hayman and Mosse, 71) that in one soil the external mycelium was exceptionally vigorous while in another it seemed to be chiefly in the rhizoplane with a ^e restricted spread in the soil. In agar culture (Mosse and Phillips, 71) the external
6 46 D. S. HAYMAN AND B. MOSSE mycelium can be greatly stimulated by adding certain substances to the medium and under these conditions hyphae grow vigorously up to 4 cm from the root surface. This is considerably more than the depletion zone around roots in the soil which is considered to extend over millimeters rather than centimeters. Sanders and Tinker (71), having considered possible mechanisms that might account for the increased phosphorus uptake of mycorrhizal roots, also concluded that it was most likely linked to the external mycelium. Baylis' (70) observation that plants lacking root hairs tend to benefit more from mycorrhizal infection would also fit in with this explanation. But so far the evidence is largely circumstantial and more positive evidence is required. The best so far is provided by the work of Stone (49) with ectotrophic mycorrhiza. He showed that in two different soils Sudan grass grown together with mycorrhizal pine absorbed very little phosphorus and grew very poorly, but it absorbed between three and ten times as much phosphorus and grew much better when the pine was not mycorrhizal. The nonmycorrhizal pine absorbed little phosphorus and grew very badly. Clearly the Sudan grass and the pine competed for a limited amount of phosphate and when the pine was mycorrhizal it obtained a much greater share. Little is said about the mycorrhizal status of the Sudan grass, but similar kinds of experiment, using either a conifer or an Angiosperm that does not form VA mycorrhiza as index of available phosphate, might be informative. Another approach would he to restrict growth of the external hyphae by treating the soil with a mild fungicide or an antibiotic. The conclusion that the external mycelium of VA mycorrhiza can act as additional absorbing surface for the host plant is so far-reaching that it cannot be accepted without further direct evidence. ACKNOWLEDGMENTS We thank Drs D. S. Jenkinson, F. Sanders and B. Tinker for helpful discussions, and Mr P. H. Le Mare and Miss B. Messer for some of the analyses. REFERENCES BAYLIS, G. T. S. (67). Experiments on the ecological significance of phycomycetous mycorrhizas. New Phytol., 66, 231. BAYLIS, G. T. S. (70). Root hairs and phycomycetous mycorrhizas in phosphorus-deficient soil.?' Soil, 33, 713. BowEN, G. D. & THEODOROU, C. (67). Studies on phosphate uptake by mycorrhizas. Proc. int. Un. for. Res. Orgn., 14th, Munich, 5, 116. DAFT, M. J. & NICOLSON, T. H. (66). Effect oiendogone mycorrhiza on plant growth. New Phytol., (>Si 343. GERDEMANN, J. W. (68). Vesicular-arbuscular mycorrhiza and plant growth. A. Rev. Phytopath., 6, 3')7' GRAY, L. E. & GERDEMANN, J. W. (69). Uptake of phosphonjs-32 by vesicular-arbuscular mycorrhiza. PL Soil, 30, 415. HARLEY, J. L. (69). The Biology of Mycorrhiza. Leonard Hill, London. HAYMAN, D. S. & MOSSE, B. (71). Plant growth responses to vesicular-arbuscular mycorrhiza. L Growth of Endogone-\noc\i\2AeA plants in phosphate-deficient soils. New Phytol., 70,. MOSSE, B. & BOWEN, G. D. (68). A key to the recognition of some Endogone spore types. Trans. Br. mycol. Soc, 51, 469. MOSSE, B. & PHILLIPS, J. M. (71). The influence of phosphate and other nutrients on the development 01 vesicular-arbuscular mycorrhiza in culture. J. gen. Microbiol, 68 (in press). MURDOCH, C. L., JACKOBS, J. A. & GERDEMANN, J. W. (67) Utilization of phosphorus sources of different availability by mycorrhizal and non-mycorrhizal maize. PI. Soil, 27, 329. NICOLSON, T. H. (i960). Mycorrhiza in the Gramineae. IL Development in different habitats, particular sand dunes. Trans. Br. mycol. Soc, 43, 132. NICOLSON, T. H. (67). Vesicular-arbuscular mycorrhiza a universal plant symbiosis. Sci. Prog., Ox; 6
7 uptake of labile P from soil 47 SANDERS, F. E. & TINKER, P. B. (71). Mechanism of absorption of phosphate from soil by Endogone mycorrhizas. Nature, Lond., 233, 278. STONE, E. L. (49). Some effects of mycorrhizae on the phosphorus nutrition of Monterey pine seedlings. Proc. Soil Sci. Soc. Am., 14, 340. SuTTON, C. D. & GuNARY, D. (69). Phosphate equilibria in soil. In: Ecological Aspects of the Mineral Nutrition of Plants (Ed. by I. H. Rorison). Brit. ecol. Soc. Symp. No. 9, 127.
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