PHOSPHATE ABSORPTION BY PLANTS FROM HABITATS OF DIFFERENT PHOSPHATE STATUS
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1 New Phytol. (1) 8, -20. PHOSPHATE ABSORPTION BY PLANTS FROM HABITATS OF DIFFERENT PHOSPHATE STATUS I. ABSORPTION AND INCORPORATION OF PHOSPHATE BY EXCISED ROOTS BY H. NASSERY* AND J. L. HARLEY Department of Botany, Sheffield University {Received 10 July 18) SUMMARY In an attempt to elucidate the mechanisms involved in the differential growth response to phosphate of four ecologically distinct species, the rate of uptake and the incorporation pattern of labelled phosphate by their excised roots v?ere investigated. No sufficiently striking or consistent difference was found in the rate of uptake or the pattern of esterification to explain their differences in response to phosphate. Calcium ions were found to stimulate uptake of phosphate by the excised roots of the four species, but neither could this effect be interpreted to explain the differential growth response to phosphate. The effect of calcium appeared to be to decrease both the permeability of, and the negative charges on, the root. INTRODUCTION The level of phosphate supply in the soil may be an important consideration in the growth of crop plants and a factor determining ecological distribution of plants in natural and semi-natural habitats (see for instance Russell, 11; Pigott and Taylor, 1). The mechanisms by which the differences of behaviour of different kinds of plant are brought about have often been sought using dry weight measurements and the appearance of deficiency symptoms to assess responses, but no general hypotheses of mechanism have yet been formulated. Genetical differences between varieties which affect the morphology and geometry of the root system seem to be important in some cases (Vose 13; Epstein and Jeffries 1) but are probably not of general significance. We have followed the work of Rorison (17), who experimented with plants from difi^erent habitats in culture solutions of different phosphate level. Amongst his experimental plants Urtica dioica and Rumex acetosa responded with greatly increased relative growth rate to increases in phosphate level between io~* M and io~^ M. The growth of Urtica was exceedingly poor and slow at the lowest phosphate levels in the culture solution. Scabiosa columbaria showed great increase up to io^^mor IO~'^M phosphate but was unaffected at higher levels. Deschampsiaflexuosashowed the least change of relative growth rate over the range and none above io"'*' M phosphate. In this paper we are concerned with the comparative rates of uptake and the pattern of incorporation of phosphate in the excised roots of these plants in short-term experiments, in order to see whether there are significant differences in the primary uptake process which might warrant further investigation. Some effects of ph and calcium ions on the process are also described. * Present address: Biology Department, Pahlavi University, Shiraz, Iran,
2 1 H. NASSERY AND J. L. HARLEY MATERIALS AND METHODS Seed collected in the Sheffield area was germinated on damp filter paper in petri dishes. The seedlings were transferred to glass jars containing continuously aerated culture solution which had the following composition: Ca(NO3)2(2 mm), KNO3(2 mm), NHNO3(i mm), MgSO(i mm), Fe Na EDTA (o.i mm), with the following micronutrients: MnS0 H2O (2.02 mg/litre), H3BO3 (2.8 mg/litre), (NH)Mo7O2 H2O (0.18 mg/litre), ZnS0 7H2O (0. mg/litre), CUSO 5H2O (0.328 mg/litre). Phosphate was added as KH2PO to provide the required concentration (10"^ M). The ph was adjusted to.5 by the addition of HNO3 and the culture solutions were renewed twice weekly. The plants were grown in a glasshouse and illuminated by fluorescent light for 12 hours per day. The plants were harvested after - months under these standardized conditions; their roots were excised and circulated in aerated distilled water for i hour before use. Tips of 1-3 cm were excised and, after blotting, placed in the experimental solutions either in shaken conical fiasks or in sintered aeration tubes. The experimental solutions contained the required concentration of KH2PO labelled with ^^P ( /ici/litre) at ph.5 unless otherwise stated. A maximum of i g of fresh roots were immersed in 500 ml of solution during most of the experiments which were carried out at 20 C for periods of time up to 3 hours. The methods of extraction and separation of the ^^P labelled compounds were those originally described by Loughman and Martin (157). The total uptake from solution was estimated by wet ashing the plant material. The digest was made up to 10 ml with H3PO, or further diluted and a io ml aliquot taken, for counting in an M liquid counter tube. Chromatograms of labelled compounds were scanned with an IDL automatic chromatogram scanner. The peaks obtained were matched with corresponding autoradiographs, the percentages of inorganic phosphate hexosephosphates, phosphoglyceric acid and soluble nucleotides were calculated after background correction. RESULTS Uptake of phosphate It was observed in a first experiment that the uptake of phosphate from 10"^ M 2^^P0 by root tips of Deschampsia and Urtica were similar over a period of 3 hours. Their uptakes were therefore compared together with those of Scabiosa from four different phosphate concentrations and the results are shown in Fig. i. There is no significant difference between the uptakes on a dry weight basis of Urtica and Deschampsia, but those of Scabiosa are much less at all concentrations. The effect of the nutrients in the culture solution used for growing the seedlings, upon phosphate uptake, was examined using Scabiosa. As Table i shows, uptake was greatly increased by the macronutrients applied at the concentrations given in the methods section. By using each of the macronutrients separately at2xio~^mit was shown that the stimulating effect was mainly due to calcium and that calcium stimulated the phosphate uptake of all the species used. Table 2 shows the effects of 10"^ M and 10"^ M CaCl2 upon uptake of phosphate by Urtica dioica, Rumex acetosa, Scabiosa columbaria and Deschampsiafiexuosa. In all species phosphate uptake is stimulated at ph.5 by calcium but a higher concentration is needed with Scabiosa and Deschampsia than with Urtica and Rumex.
3 Phosphate absorption. I 15 The effect of ph upon the stimulation of phosphate uptake by calcium was investigated using a range of ph values between 3 and 7. The solutions were adjusted by means of M KOH and M KCl to have the required ph value and a K"^ concentration of. X 10 * M. The ph values measured before and after the experiment showed no l500r ' 10' MKH2P0 Fig. I. Uptake of phosphate by excised roots at 20 C, ph.5., Urtica; k, Scabiosa; A, Deschampsia. S.E. of mean less than 5% of mean if not shown. Table i. The effect of macro- and micronutrients upon phosphate uptake by excised roots of Scabiosa atph.s, 20 C Solution IO jtvrl2 Jr*J IO" KH^32pQ^ + micronutrients IO KH^32pQ^ _j_ macronutrients IO ~ IvHz^^PO^ + fuil nutrients /jg P/g dry weight/3 hours Duplicates Mean II-I significant change. Fig. 2 shows the effect of ph upon phosphate uptake by Urtica in the presence and absence of i o ~ ^ M CaClj. The stimulation is greater above ph and calcium appears to shift the optimum from around.5 to.0. With Deschampsia and Scabiosa which showed little effect of 10"^ M CaCl2 at ph.5 a definite stimulation of uptake by calcium was observed at ph 7 (Table 3) B N.P.
4 i H. NASSERY AND J. L. HARLEY Table 2. The effect of calcium chloride on phosphate uptake from 10"^ M KH2PO by excised roots at ph.5, 20 C Species Urtica Rumex Scabiosa Deschampsia CaClj (M) o 10 ~^ 10"^ o 10 ~^ IO~^ o 10-^ 10"^ o IO -^ IO ~^ fig p/g dry weight/3 hours Duplicates Mean 11 i II /o stimulation _ Since in Rorison's (17) experiments Urtica, a plant of base rich soil, exhibited a very low relative growth rate below 10"^ M phosphate and a great increase with increasing phosphate concentration, the effect of cations upon its phosphate economy was examined in further detail. Table shows that calcium ions stimulate its uptake at 10 ~ and 10 " ^ M phosphate but not significantly above this level, that is the effect is greatest at concentrations where growth is slow and phosphate deficiency symptoms may be observed. Table 5 oor 300 A > Fig 2. Effect of ph on the uptake of phosphate by roots of Urtica from to-' M KH PO m the presence (A) and absence ( ) of 10"=' CaCl2. Duplicate values given. * 5 ph
5 Phosphate absorption. I 17 further shows that in io~^ M phosphate uptake is stimulated by several cations to differing degree if present at io~^ M. The divalent ions calcium and, to a lesser extent, magnesium stimulate phosphate absorption much more than do potassium and sodium. Since the net uptake of phosphate is stimulated by cations, calcium ions in particular, it was of interest to determine whether any part of the stimulation was due to a reduction Table 3. Mean values of phosphate uptake by excised roots of Deschampsia and Scabiosa in a range ofph values with and without lo"^ M CaCl2 at 20 C {values as fxg P/g dry weight/^ hours) ih Control aos 305 Deschampsia 10 ~^ CaCl Scabiosa Control 10 -' CaCl Table. The effect of 10 ^ CaCl2 upon the uptake of phosphate by XJrtica. from solutions of potassium phosphate of different concentrations {ph.5, 20 C) KH2"PO (M) Mean /ig P/g dry weight/3 hours % Control With 10 "^ CaCU increase 10 ~ ~' "* 52 0 IS 10 ~^ Table 5. The effects of io~^ M solutions of different cations upon phosphate uptake by excised Urtica roots of io~^ M phosphate {ph.5, 20 C) Phosphate supplied Added salt Uptake pg P/g dry weight/3 hours NaH2PO o 120 NaCl ISO KH2PO o 120 KCl 20s in efflux. The uptake from 10"^ M KH2^^P0 was measured as described before at 20 C. After the uptake period the roots were quickly washed in 5 x 100 ml of cold (5 C) distilled water. They were then transferred to 10 ml of one of the following solutions at 5 C; distilled water, 10"^ M KCl or 10~^ M CaClz. The radioactivity in the washing solution was measured after 2 hours. The efflux was reduced to one-half in the presence of calcium chloride (Table ). In a second experiment uptake and efflux of phosphate were both measured in the presence and absence of calcium or potassium at 5 C. The results are shown in Table 7. CaCla stimulates uptake at 5 C as it does at 20 C. Moreover although the total uptake is not more than one-fifth of the uptake at 20 C, the proportion of phosphate lost during
6 i8 H. NASSERY AND J. L. HARLEY the washing phase is similar. It is therefore concluded that the phosphate which is lost under these conditions is not likely to be associated with the cell walls, since, if it were, one would expect quantitatively similar losses at C and 20 C. A part of the eftect of calcium on net uptake may therefore be the result of reduced efflux. Table. Effect of cations on efflux of phosphate from excised roots of Urtica {uptake from io~^ M KH^^^PO^ at 20 C, ph.5, 3 hours; followed by washing 2 hours in the solution stated at f C) Washing solution Distilled water 10-3 MKCI 10-3 M CaCI, Absorbed phosphate remaining after washing (//g/g dry weight) Efflux Total (counts/min/mg) %of uptake -5 Table 7. Effect of cations on the uptake and efflux of phosphate of Urtica roots at ^ C {uptake from 10"^ at 5 C,pH p.5 in 3 hours, in the presence and absence of KCl or CaCl2; efflux into water, KCl or at 5 C) Salt present during uptake and washing None 10-3 M KCl 10-^M CaCl, fig P/mg dry weight absorbed in 3 hours %of C/min lost Table 8. Uptake and distribution of labelled phosphate at short time intervab (10"^ ^, at 20 C, ph.5; soluble phosphate extracted with cold o.i N perchloric acid) Vrtica Plant Deschampsia Rumex Scabiosa Minutes uptake I 2 8 I 2 8 I2 8 I2 8 Uptake //g/g dry weight Total -Ca +Ca II.O I.O 2-5 IO.O II.O II.O soluble -Ca +Ca Distribution of ^^ in soluble fraction Inorganic P Su ar P Nucleotide P (%) (%) (%) -Ca +Ca -Ca +Ca -Ca +Ca io IO IO II zo IO 2 0 2S i 2 SS i IO
7 Phosphate absorption. I 1 The pattern of esteriflcation in excised roots A series of short-term experiments were performed with rephcate samples to determine the uptake of phosphate from 10"^ M KH2^^P0 and the pattern of esterification. The results are summarized in Table 8. In case of Urtica the effect of io~^ calcium chloride on esterification were also observed. The percentage distribution of labelled phosphate compounds are similar in Urtica, Deschampsia and Rtimex and are in general agreement with those reported for other plant materials (e.g. Loughman and Scott Russell, 157) but the percentage of labelled inorganic phosphate was very much greater in Scabiosa than in the other species. Calcium ions had little effect on the esterification pattern of Urtica. DISCUSSION In this paper uptake of phosphate by excised root apices has been examined to determine whether the explanation of the differences in behaviour of Urtica dioica, Deschampsia flexuosa, Rumex acetosa and Scabiosa columbaria in response to phosphate supply is likely to be found in differences of primary uptake mechanism. It seems that the roots of the extreme species Urtica dioica and Deschampsiaflexuosashow no differences in the rate of uptake over wide ranges of concentration from io~ toio"^m and their patterns of esterification at io~^ M phosphate are similar. Rumex acetosa seems to agree in behaviour with these two species but Scabiosa columbaria has a slower rate of uptake and incorporates the phosphate absorbed more into inorganic phosphate in the initial phases. It is therefore concluded that differences in uptake or esterification estimated in the ways employed do not afford any sim.ple explanation of the differences in ecological behaviour nor provide any clearly profitable line of attack upon the problem of its causation. 5. columbaria as grown for these experiments differs in its root morphology particularly in the absence of root hairs. The stimulation of net phosphate uptake by calcium has also been observed by many others (e.g. Hyde, i0). It does not seem to be specific to calcium ions since magnesium ions and to a lesser extent those of potassium and sodium stimulated uptake by Urtica. The fact that the stimulations are greater at high ph values in Urtica and were only observed at ph 7 with other species suggest a similar explanation to that given by Hyde (i0) and Jermings (1) that they result from a decrease of negative charges on the root surface. The reduction of efhux of phosphate from Urtica roots in the presence of calcium leads also to the conclusion that calcium affects the permeability of the cells to phosphate. The fact that calcium only affects the uptake by Urtica significantly in those concentrations of phosphate shown by Rorison (17) to support very low relative growth rates in Urtica in contrast to the other species might possibly have some ecological relevance. REFERENCES EPSTEIN, E. & JEFFERIES, R. L. (1). The genetic basis of selective ion transport in plants. A. Rev. PL PhysioL, 15,. HYDE, A. H. (i0). Factors controlling the absorption of phosphate from dilute solutions by intact roots. E). Phil, thesis. University of Oxford.,,,,., JENNINGS, D. H. (1). The effect of cations on the absorption of phosphate by beech mycorrhizal roots. New Phytol., 3, 38. LOUGHMAN, B. C. & MARTIN, R. P. (157). Methods and equipments for the study of the incorporation of phosphorus by intact barley plants in experiments of short duration, y. exp. Bot., 8, 272. LOUGHMAN, B. C. & SCOTT RUSSELL, R. (157). The absorption and utilization of phosphate by young barley plants, y. exp. Bot., 8, 280.
8 2O H. NASSERY AND J. L. HARLEY PiGOTT, C. D. & TAYLOR, K. (1). The distribution of some woodland herbs in relation to the supply of nitrogen and phosphorus in the soil. J. Ecol. (Suppl.), 52, 175. RORISON, I. H. (17). A seedling bioassay on some soils in the Sheffield area. J. Ecol., 55, 725. RUSSELL, E. J. & RUSSELL, E. W. (11). Soil Conditions and Plant Growth, th edn. Longmans, London. VoSE, P. B. (13). Varietal differences in plant nutrition. Herb. Abstr., 33, i.
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