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Uptake and translocation of Sr by Zea mays
Radiation Botany, 1973, Vol. 13, pp. 273 to 281. Pergamon Press. Printed in Great Britain.
UPTAKE AND T R A N S L O C A T I O N OF Sr BY ZEA MAYS* R. I-IANDLEY a ~ d K. L. B A B C O C K
Department of Soils and Plant Nutrition, University of California, Berkeley, California 94720, U.S.A.
(Received 19 iPlarch 1973; revised) HA-NDLEY R. and BABCOCKK. L. Uptake and translocation of Sr by Zea mays. Radiation Botany 13,
273-281, 1973.--The uptake of Sr by maize-root segments representing the whole root system is strongly temperature dependent but a large non-metabolic component apparently involving adsorption within the cell membranes is indicated. About 60 per cent of the Sr taken up under conditions permitting metabolism is resistant to elution. K in the ambient solution at a concentration amounting to 20 per cent of the Sr concentration essentially abolishes metabolic uptake. Non-metabolic Sr uptake is little affected by this K concentration. The inhibitory effect of Ca on Sr uptake is less than that of K and largely exerted on the non-metabolic phase. This inhibitory effect is countered to some degree by the ability of Ca to hinder the entry of Sr into the xylem and so its loss via the cut ends of the root segments. In whole-plant experiments K depressed root concentrations of Sr more than shoot concentrations indicating that the inhibition is exerted mainly at the tonoplasts of cortical cells. Ca had a smaller effect than K which was mainly evident in greater root retention of Sr. INTRODUCTION
THE RESULTS o f w o r k done in this laboratory(7,8) and those reported by MAAS07) indicate that the roots of maize differ from those of most other crop plants with respect to the uptake of Ca and Sr in that a large fraction of the total uptake of these ions appears to be metabolically mediated. Whether or not this is unique to the maize root is questionable but Ca uptake by the excised roots of other crop plants investigated has been found to be independent of temperature and the presence of metabolic inhibitors and so to involve only physical processes.(3,4,1s) In work reported in 1972 (s) dealing with the translocation of fallout radionuclides in 3 crop plants (bean, tomato, and corn) it was found that in all 3 species root retention of ~3~Gs exceeded that of s6Sr. Since Cs is metabolically accumulated by the roots of all these plants its lower mobility (root-shoot) could be ascribed to the low availability for upward transport of Cs seques-
tered in vacuoles of the root cortex. Because of the ability of the maize root to absorb Sr metabolically and, as will be shown here to retain it against elution, one might expect Sr translocation to be similarily restricted in this plant. However, although root retention of Sr was greater than in bean or tomato, Sr in maize was very mobile compared to Cs. The maize plants were sampled immediately after a 4-day treatment in dilute (I/4 Hoagland) solutions contaminated with SSSr or xsvCs and again after being allowed to grow for 22 days in uncontaminated solution. During this latter period the fraction of the SSSr held by the root declined from 51.2 per cent of the total to 13.9 per cent, while the distribution of lSTCs between root and shoot remained constant. These results were obtained with maize plants growing in complete culture solutions whereas the ability of excised maize roots to absorb Sr and Ca metabolically has only been demonstrated in the absence of competing
* This report is based on work performed under Contract AT-(04-3)-34, PA 23 with the United States Atomic Energy Commission. 273
274
R. HANDLEY and K. L. BABCOCK
ions. For this reason a new study of Sr uptake and translocation by maize was undertaken with emphasis upon the influence of other ions upon metabolic and non-metabolic uptake by excised roots and the relation of these effects to the upward translocation of Sr in intact plants. The interfering ions selected were Ca, because of its chemical similarity to Sr, and K which M.A~(17) has demonstrated to inhibit Ca uptake by excised maize roots. MATERIALS A N D M E T H O D S
The excised-root material was obtained by germinating maize seed (yea mays L. var. Golden Cross Bantam) in running tap water overnight and subsequently supporting it on open-weave cheesecloth over an aerated solution 0.1 m M in Ca(NO3)z, K H 2 P O 4 and M g S O 4 for 5 days at 26°C in darkness. A 4-I. beaker was used for 100 seeds, the liquid level being about 1 cm below the cloth. A polyethylene bag used as a cover to maintain a humid atmosphere was removed on the third day. The roots of 200 plants were excised on the fifth day at the seed and segments about 1 cm long were cut into 2 liters of water. After mixing, the root material was filtered off on a sieve of cotton towelling, washed with 3 liters of water and finally freed of excess water by applying vacuum. Samples of 1.00 g fresh weight were used with a solution "volume of 1-0 1. Root samples were separated from the experimental solutions using W h a t m a n No. 541 paper and vacuum. Before analysis the samples were rinsed with water, dried at 60°C and weighed. Sr uptake was determined using SrCI~ solutions (0.005 N) labelled with 85Sr (4.0 ~Ci per liter) and standard techniques. K and Ca were determined by absorption spectroscopy after ashing and solution of the ash. Except where otherwise indicated all figures presented represent averages of 3 or more determinations. For the experiment with whole plants, maize seed was germinated and grown for 3 days in dilute culture solution as described above. T h e n 54 seedlings with roots about 10 cm long were transplanted into 1/10 strength Hoagland solution. T h e plants were supported on perforated lids made of wax-impregnated plaster of Paris resting on white plastic flower pots (J. M.
McConkey Inc. Puyallup, Washington) of about 3-1. capacity. Each of 18 pots held 3 plants. The pots were wrapped with aluminum foil to exclude light. The experiment was carried out after the plants had grown thus in the greenhouse with aeration for 2 weeks. At that time the dilute culture solution in each pot was replaced by the appropriate experimental solution after thorough washing of pots and roots in running water. T h e SrCI~. solutions were 0.005 N. T h e KCI and CaC12 solutions were 0.001 N. All solutions were labelled with 20 [zCi of SsSr per liter and were aerated. T h e total volume in each pot was 2.5 1. After 24 hr and after 40 hr the plants in 9 pots were harvested. The roots were washed in running distilled water and the plants were separated into root and shoot fractions. These were dried for several days at 60°C, weighed and then ground using a Wiley mill and the 20 mesh screen. Weighed samples were then counted using a well-type scintillation detector (Tracerlab Model SC-54) and a g a m m a spectrometer (Tracerlab Model SC-78) with a window width of 2.0 V. The standards consisted of 2"00 ml samples of the well-stirred experimental solutions taken just prior to introduction of the plants. The plants taken for analysis at both sampling times were healthy in appearance with no evidence of injury. RESULTS AND DISCUSSION
Uptake of Sr by excised roots over a 5-hr period at 26°C and at I°C is shown in Fig. 1. The amounts of Sr absorbed by this material were much less than those found in earlier workCn) where newly vacuolated tissue close to the root apex absorbed about 30 mequiv per kg fresh weight in 5 hr at 26°C. T h e corresponding figure for the whole root used in these experiments was only about 7.5 mequiv per kg. This was to be expected since the material used here was overwhelmingly composed of mature cells which are well known to be less active in salt uptake than those immediately proximal to root meristems. T h e amounts absorbed at 26°C were only slightly less than those reported by M,~m(17) for Ca uptake by 6-cm apical segments of maize roots of the deKalb variety but the uptake of Sr at low temperature was greater and at 5 hr amounted to 60 per cent of that taken up at 26°C.
UPTAKE AND TRANSLOCATION OF Sr BY ZEA MAI'i~
275
5oL o
5O
u3
0
I
I
I
l
]
~
2
3
4
5
Time tn hours
FIO. 1. Uptake of Sr by root segments of maize from 0.005 N SrCI2 at 26°C and at I°C (lower curve). Thus although a pronounced temperature effect was found with segments representing the whole root a relatively large non-metabolic component was indicated. At 5 hr in the cold the tissue was not yet in a steady state with the external solution. Sr entry was continuing albeit at a slow rate. This strongly suggests passage through a barrier presumably the plasmalemma which limxts the rate of entry. T h e curve presented by M~t~ts(17) for Ca uptake at low temperature is similar in this respect. It is possible of course that imposition of a low temperature alters the permeability of the plasmalemma but the ability of plants such as barley, OS) for which no metabolic uptake of Ca can be demonstrated in excised roots, to transport Ca to the shoot argues that the plasmalemma is normally permeable to alkaline earth cations. U p w a r d transport implies entry into the symplasm. (2,s) Uptake of Sr at 1°C is accompanied by loss of native K. K loss represents about 80 per cent of the Sr taken up in 5 hr. No loss of native Ca occurs. At 26°C no loss of either K or Ca was detected. Possibly at the higher temperature K displaced from cell wall and cytoplasmic binding sites is metabolically sequestered in vacuoles rather than being released to the solution. T h e design of these experiments does not
permit any evaluation of the amounts of Sr which m a y be lost from the cut ends of the root segments after absorption. At l°C these are probably close to nil since several studies( 4, s, 7,1416,10) have shown release of ions into the xylem to be under metabolic control. Therefore while the curve shown in Fig. 1 for uptake at I°C probably represents passive uptake accurately, the amounts of Sr absorbed indicated for various times at the higher temperature m a y be erroneously low. There appears to be no simple way to eliminate this possible error. Use of longer root segments or even whole roots cut only at the seed would not eliminate it since the data of EVANS(7) indicate that the amounts of Ca exuded by maize-root sections are a linear function of the segment length exposed to the solution containing Ca. Solution of this problem will require experiments designed to measure both uptake and exudation. Methods for this purpose have been designed by EvANs(7) and by MooRE et al.(10) but apparently have not been extensively used as yet. The data of Table 1 indicate that a large fraction of the labelled Sr taken up at 26°C is resistant to removal by unlabelled SrC12 solutions. For these experiments the root samples were allowed to take up Sr from SrC12 solutions
276
R. HANDLEY and K. L. BABCOCK Table 1. Lossfrom excised roots of absorbed Sr labelled with s6Sr to unlabeUedSrClz*
Sr, ~tequiv/g, dry wtq-S Before After elution elution
Uptake solution
Elution temperature
Sr*CI2 0.005 N
26°C
144+7
84+5
58
Sr*C12 0.005 N
I°C
144+7
94::k6
65
Sr*C19. 0.005 N + CaCI~ 0:001 N
26°C
118+9
70+5
59
Sr*C19. 0"005 N + CaC19. 0.001 N
I°C
118+9
69+4
59
% retention
* 5-hr absorption period, 5-hr elution period. labelled with SSSr for 5 hr and were then transferred after brief rinsing for a further 5 hr to urdabelled solutions of the same concentration (0-005 N). About 60 per cent of the Sr taken up remained with the tissue after elution. This indicates a site of Sr accumulation deeper in the cell than the plasmalemma since this m e m b r a n e appears permeable to Sr. This site is probably at the tonoplast since previous work(10-a2) has shown accumulation of Na, Ca and Sr by maize roots to occur coincidentally with the appearance of well-defined (i.e. membranelimited) vacuoles. Whether or not the plasm a l e m m a is also active in Sr accumulation is not apparent. Note that the concentration of Sr (0.005 N) used in these experiments is well above that at which the first or high-affinity mechanism described by EPSTEIN(5,e) for the uptake of monovalent ions becomes saturated. This mechanism m a y exist at the plasmalemma. The data of MnAst 17) indicate such a mechanism to be operative in Ca uptake by maize roots. However the resistance to elution of Ca absorbed from solutions of very low concentration (0.010.2 mequiv per 1.) was not reported. T h e data of Table 1 and Fig. I indicate that
the concentration of labile Sr (i.e. presumably that physically bound on cell walls and in the cytoplasm) is lower when operation of the vacuolar uptake mechanism is permitted. While the 5-hr uptake at I°C is 60 per cent of that taking place at 26°C (Fig. 1), only about 40 per cent of the Sr taken up at 26°C is readily elutable. Subtraction of the uptake at I°C from that at 26°C would in this case yield an erroneously low estimate of the metabolically absorbed fraction. Losses of Sr via xylem exudation as well as sequestration of Sr in the vacuoles probably contributes to this effect. Penetration of the plasmalemma appears to be the rate-limiting step in Sr uptake at this concentration. T h e effects of increasing K concentrations upon the 5-hr uptake of Sr at 26°C and at I°C are shown in Fig. 2. At 26°C relatively low concentrations of K inhibit Sr uptake strongly. Addition of 1.0 mequiv per 1. of K to the 0'005 N SrC12 solution (equivalent per cent K = 1 6 . 7 ) caused a 40 per cent reduction in Sr uptake. At higher concentrations of K a linear relationship between Sr uptake and K concentration obtains. With metabolism suppressed by lowering the temperature to I°C the effect
UPTAKE AND TRANSLOCATION OF Sr BY ZEA I14AYS
277
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75
c
o.
5O
25
I
0
15
I 30
I
I
I
45
60
75
Equivolent percenl K in solulion
FIO. 2. Effect of K on the 5-hr uptake of Sr by root segments of maize at l°C and at 26°C (lower curve). Sr concentration 0.005 N. of K is greatly reduced and the relationship is linear over the range of K concentration used. It appears that at relative K concentrations above about 25 per cent the metabolic phase of Sr uptake is virtually elilrfinated and that further additions of K are solely effective in reducing the non-metabolic phase by competition for cytoplasmic and cell-wall binding sites. Note that the linear portion of the graph obtained at 26°C parallels the straight line obtained for K interference at 1°C. T h e data of Fig. 2 suggest that the metabolic process responsible for Sr accumulation is the same as that for K and that K is greatly preferred over Sr. The results obtained by MAAS(17) for Ca uptake by maize roots indicate that the same mechanism also accepts Ca. However, with maize roots as with the excised roots of other plants Sr and Ca exert stimulatory rather than inhibitory effects upon K uptake (Table 2, 9) and it is apparent that more than simple competition for a common carrier is involved. It m a y be that Sr inhibits the transfer of K to the xylem and so its loss to the solution via the cut ends of the root segments. We have observed that the presence of Ca in the medium very strongly inhibits Cs transloeation to the shoot of maize. T h e interaction of Sr and K in this regard would be expected to be similar. These data have not been published as yet.
Table 2. Effect of Sr on K uptakefrom 0"005 N KCl
Sr, mequiv per 1.
Sr, equiv %
0 1.0 3.0 5.0 7.0 10.0
0 16"7 37.5 50-0 58.4 66"5
K uptake, tzequiv]g K uptake, (dry)* % of control 232 247 259 274 289 284
100 106 112 118 124 122
* Average value, 2 determinations. The effects of increasing concentrations of Ca upon Sr uptake at 26°C and at I°C are shown in Fig. 3. Unlike K, Ca inhibited Sr uptake more effectively at I°C than at 26°C. Indeed, concentrations of Ca up to about 10 equivalent per cent had no significant effect upon Sr uptake at 26°C. Above this level Sr uptake declined linearly with Ca concentration. At 1°C a linear relationship obtained over the range of Ca concentrations tested. T h e total effect of Ca upon Sr uptake by excised roots thus appears to involve both stimulatory and inhibitory factors. T h e inhibitory factor is exerted principally at least upon the non-metabolic phase of Sr uptake through competition for adsorption
278
R. HANDLEY and K. L. BABCOCK
t00
E 75
o. 50
25
I t0
0
I 20 Equ~volenl
percent
I 30
I 40
I 50
Co in s o l u t i o n
FIO. 3. Effect of Ca on the 5-hr uptake of Sr by root segments of maize at 26°C and at I°C (lower curve). Sr concentration 0.005 N. sites. Note that the straight-line portions of the graphs obtained at 26°C and at 1°C are nearly parallel. The stimulatory factor which, at low relative concentrations of Ca, is able to negate this inhibition does not appear to be exerted at the tonoplast. The presence of Ca in the medium had no effect upon the retention of absorbed labelled Sr by excised root segments against elution by an unlabelled solution (Table 1). That is, the presence of Ca did not affect the distribution of Sr between the labile phase and the sequestered phase which we postulate to
reside in the vacuole. Rather it appears to be exerted upon the metabolic transfer of Sr to the xylem. The experiments with whole plants described below tend to support this interpretation. The implications of Figs. 2 and 3 are perhaps somewhat more clearly evident in the data shown in Table 3. To obtain these data the 3-hr and 5-hr uptake of Sr from 0.005 N SrC12 was measured using the pure solution and solutions containing 1"0 mequiv of CaC1,. or KC1 per liter. Measurements were made at I°C and at 26°C. The data indicate that at
Table 3. Effects of Ca and K on Sr uptake by excised rootsfrom 0.005 aV SrCI~
Expt. no.
Time, hr
Interfering ion*
5 5 6 6 7 7 8 8
5 5 3 3 5 5 3 3
None Ca None Ca None K None K
* Interfering ion cone. = 1.0 mequiv/1.
26°C
I°C
Uptake at 26°C, % of control
134.0-t-4.9 121.1 4-0.9 104.5 4-1.9 90.64-0.7 130.0-t-2.5 80.5-4-1.7 116"8:tz3.4 71"2 -t-2.8
79"4-t-0.8 66.7 4- 1.0 72"1 4-1-7 59.9 4-0.9 84.54-1.6 79.9 4- 0.5 70.3 4-0"3 70-6 4-1.1
100 90.4 100 86.7 100 61-7 100 60"9
Av. Sr uptake izequiv/g, dry wt 4- S
Uptake at I°C, % of control I00 84.0 100 83.1 100 94.6 100 100.4
UPTAKE AND TRANSLOCATION OF Sr BY ZEA MA ]':S' the concentrations of Sr and interfering ions used the inhibitory effect of K is exerted almost entirely upon the metabolically mediated phase of Sr uptake and that of C,a upon the nonmetabolic phase. Note that, although the total inhibitory effect of Ca (i.e. the effect at 26°C) is much less than that of K, the ability of Ca to reduce the non-metabolic phase exceeds that of K. This is of course to be expected in view of the higher adsorption energy of the divalent ion. Ca appears to be only weakly competitive with Sr for metabolic uptake. Note however that the competitive ability of Ca at the tonoplast would be partially masked if, as postulated above, Ca exerts an inhibitory effect upon transfer of Sr to the xylem. The effects of K and Ca on the uptake and distribution of Sr by whole maize plants are seen in Table 4. Two effects of K are evident: (1) a reduced total uptake and (2) a pronounced reduction of the root-shoot concentration ratio. The data obtained with excised roots would lead one to expect a sharply reduced Sr uptake by the
279
root when K is present in the medium. However if the inhibitory effect of K were exerted at the tonoplast only, reduction of the amount of Sr found in the shoot would not be expected. The resistance of metabolically absorbed (i.e. vacuolar) Sr to elution shown above (Table 1) suggests that Sr sequestered in vacuoles of the root cortex is only very slowly available for upward transport. In view of the reduced concentrations of Sr found in the shoots of plants receiving K it appears most likely that K also interferes with the metabolically controlled mechanism responsible for the pumping of Sr into the xylem. The location as well as the identity of this mechanism is unknown at present. The endodermis,( TM the young xylem cells themselves(1,1s) and the stelar parenchyma(5,1s,le) have been suggested as the active sites. The lowered root-shoot concentration ratios for Sr absorbed from solutions containing K and indeed the failure of K to suppress entirely the upward movement of Sr indicate that K is much less effective here than at the tonoplast in inhibiting Sr secretion.
Table 4. Effect of K and Ca on uptake and root-shoot distribution of Sr
Interfering ion
Plant fraction
Dry wt, g
None
Root Shoot Root Shoot Root Shoot Root Shoot Root Shoot Root Shoot Root Shoot Root Shoot Root Shoot
0.345 0.970 0.356 0.901 0.408 1.049 0.546 1.418 0.411 1.085 0.291 0.840 0.440 1"215 0.440 0.949 0-361 1.029
None None K K K Ca Ca Ca
Sr~ [zequiv Sr, in conc. [xequiv]g fraction 585 124 595 133 604 130 234 87 229 81 220 74 538 99 541 108 591 92
202 120 212 120 246 136
128 123 94 88 64 62 237 120 238 103 213 95
Sr, % in root
Sr, cone. ratio root]shoot Av.4-S
St, cone. whole plant ~equiv/g Av.+S
Sr, cone. whole plant % cont.
4.6±0.1
2574-11
100
2.84-0-2
1204- 9
47
5-64-0.7
2284-16
89
63 64 64 51 52 51 66 70 69
280
R. HANDLEY mad K. L. BABCOCK
We have the feeling, but at present no data to support it, that the relative inefficiency of K in this regard may be related to the preferential absorption of K by phloem tissue. This would reduce the effective concentxation of K in the vicinity of the xylem. K is moved readily in the phloem whereas Ca and Sr are largely excluded.CS) The presence of Ca, predictably in view of the results obtained with excised roots, had a smaller effect than K upon total uptake but lowered both root and shoot concentrations. The principal effect of Ca was to reduce the root-shoot translocation of Sr. The concentration of Sr in the root was lowered (as with excised roots) only about 6 per cent by the presence of Ca in the medium amounting to 16.7 per cent of the cation concentration while the Sr concentration in the shoot was lowered by 22 per cent. This suggests that the failure of relatively low concentrations of Ca to inhibit Sr uptake by excised roots at 26°C (Fig. 3) was due to a reduction in the ability of roots receiving Ca to pump Sr into the xylem. I n experiments with excised roots this effect would of course counter the inhibitory effect of Ca. As mentioned above we have found a similar though much more marked effect of Ca with respect to Cs translocation in maize. The same phenomenon was noted by JACKSONet al.~14) who reported the effects of various cations on the uptake and translocation of Cs by wheat seedlings. It would appear from this that the Viets effect,~*°) i.e. the stimulation of K, Rb and Cs uptake by Ca and other polyvalent ions by excised roots may be exerted at the stele rather than at the cell membranes or tonoplasts of the cortical cells. The data of Table 4 represent the results obtained using a 24-hr absorption period. A similar experiment using a 40-hr period yielded closely similar results. In the interest of economy these results are not presented here. The results of this work indicate that the high degree of Sr mobility with respect to root-shoot transport found for maize in the previous experiments(S) was due to 3 factors: (1) the relatively large non-metabolic component involved in Sr uptake, (2) the effect of K in reducing or eliminating Sr sequestration in vacuoles of the root cortex and (3) the relatively
smaller effects of K and Ca in inhibiting Sr uptake into the xylem. The effect of K in reducing vacuolar uptake is of particular importance in this regard since in the presence of K the ability of the maize root to sequester Sr is largely eliminated so that it behaves much as do the roots of other plants lacking this ability.
REFERENCES I. ANDERSON W. P. and HOUSE C. R. (1967) A
2. 3.
4.
5. 6.
7. 8.
correlation between structure and function in the root of Zea mays. J. Exptl Botany 18, 544-555. ARISZW. H. (1956) Significance of the symplasm theory for transport across the root. Protoplasma 46, 1-62. BnRBERD. A. and KOONTZH. V. (1963) Uptake of dinitrophenol and its effect on transpiration and calcium accumulation in barley seedlings. Plant Physiol. 38, 60-65. DREW M. C. and BmDULPHO. (1971) Effect of metabolic inhibitors and temperature on uptake and translocation of 45Ca and 42K by intact bean plants. Plant Physiol. 48, 426-432. EPSTEXN E. (1971) The upward movement of water and nutrients, pp. 151-189. In, Mineral nutrition of plants. Wiley, New York. EPSTEINE., R~INSD. W. and ELZAMO. E. (1963) Resolution of dual mechanisms of potassium absorption by barley roots. Proc. Natl Acad. Sci. 49, 684-692. EvANsE. C. III (1964) Polar transport of calcium in the primary root of Zea mays. Science 144, 174-177. I-~NDLEYR. and BABOCKK. L. (1972) Translocation of 85Sr, 137Cs and l°SRu in crop plants. Radiation Botany 12, 113-119.
9. HANDLEY R., MJ~TWALLY A. and OVERSTREET R.
10. 11. 12.
13.
(1965) Effects of Ca upon metabolic and nonmetabolic uptake of Na and Rb by root segments of yea mays. Plant Physiol. 16, 513-520. HANDLEY, R. and OV~RSTR~ET R. (1961) Uptake of calcium and chlorine in roots of yea mays. Plant Physiol. 36, 766-769. HnNDLEYR. and OV~RSTREETR. (1963) Uptake of strontium by roots of Zea mays. Plant Physiol. 38, 180-184. HAbrDLEYR., VmAJ. R. D. and OVERSTR.EETR. (1960) Metabolic and non-metabolic uptake of sodium in roots of Zea mays. Plant Physiol. 35, 907-912. HYLMOB. (1953) Transpiration and ion absorption. Physiol. Plantarum 6, 333-405.
UPTAKE AND TRANSLOCATION OF Sr BY ZEA zl~IAYS 14. JACKSONW. A., Luco H. M. and CRAIGD. (1966) Cesium uptake from dilute solutions by young wheat seedlings as affected by selected cations. Plant Soil 24, 33-53. 15. L.~UCHLI A. and EPSTEIN E. (] 971) Lateral transport of ions into the xylem of corn roots I. Kinetics and energetics. Plant Physiol. 48~ 111-117. 16. LXucrILI A., SPURR A. R. and EPSTEIN E. (1971) Lateral transport of ions into the xylem of corn roots II. Evaluation of a stelar pump. Plalzt Physiol. 48, 118-124.
281
17. MAAS E. V. (1969) Calcium uptake by excised maize roots and interactions with alkali cations. Plant Physiol. 44, 985-989. 18. MOORE D. P., JACOBSON L. and OVERSTm~.ETR. (1961) Uptake of calcium by excised barley roots. Plant Physiol. 36, 53-57. 19. MOORED. P., MASONB.J. and MARSE. V. (1965) Accumulation of calcium in exudate of individual barley roots. Plant Physiol. 441,641-644. 20. VIETSF. G. (1944) Calcium and other polyvalent ions as accelerators of ion accumulation by excised barley roots. Plant Physiol. 19, 466-480.
UPTAKE AND T R A N S L O C A T I O N OF Sr BY ZEA MAYS* R. I-IANDLEY a ~ d K. L. B A B C O C K
Department of Soils and Plant Nutrition, University of California, Berkeley, California 94720, U.S.A.
(Received 19 iPlarch 1973; revised) HA-NDLEY R. and BABCOCKK. L. Uptake and translocation of Sr by Zea mays. Radiation Botany 13,
273-281, 1973.--The uptake of Sr by maize-root segments representing the whole root system is strongly temperature dependent but a large non-metabolic component apparently involving adsorption within the cell membranes is indicated. About 60 per cent of the Sr taken up under conditions permitting metabolism is resistant to elution. K in the ambient solution at a concentration amounting to 20 per cent of the Sr concentration essentially abolishes metabolic uptake. Non-metabolic Sr uptake is little affected by this K concentration. The inhibitory effect of Ca on Sr uptake is less than that of K and largely exerted on the non-metabolic phase. This inhibitory effect is countered to some degree by the ability of Ca to hinder the entry of Sr into the xylem and so its loss via the cut ends of the root segments. In whole-plant experiments K depressed root concentrations of Sr more than shoot concentrations indicating that the inhibition is exerted mainly at the tonoplasts of cortical cells. Ca had a smaller effect than K which was mainly evident in greater root retention of Sr. INTRODUCTION
THE RESULTS o f w o r k done in this laboratory(7,8) and those reported by MAAS07) indicate that the roots of maize differ from those of most other crop plants with respect to the uptake of Ca and Sr in that a large fraction of the total uptake of these ions appears to be metabolically mediated. Whether or not this is unique to the maize root is questionable but Ca uptake by the excised roots of other crop plants investigated has been found to be independent of temperature and the presence of metabolic inhibitors and so to involve only physical processes.(3,4,1s) In work reported in 1972 (s) dealing with the translocation of fallout radionuclides in 3 crop plants (bean, tomato, and corn) it was found that in all 3 species root retention of ~3~Gs exceeded that of s6Sr. Since Cs is metabolically accumulated by the roots of all these plants its lower mobility (root-shoot) could be ascribed to the low availability for upward transport of Cs seques-
tered in vacuoles of the root cortex. Because of the ability of the maize root to absorb Sr metabolically and, as will be shown here to retain it against elution, one might expect Sr translocation to be similarily restricted in this plant. However, although root retention of Sr was greater than in bean or tomato, Sr in maize was very mobile compared to Cs. The maize plants were sampled immediately after a 4-day treatment in dilute (I/4 Hoagland) solutions contaminated with SSSr or xsvCs and again after being allowed to grow for 22 days in uncontaminated solution. During this latter period the fraction of the SSSr held by the root declined from 51.2 per cent of the total to 13.9 per cent, while the distribution of lSTCs between root and shoot remained constant. These results were obtained with maize plants growing in complete culture solutions whereas the ability of excised maize roots to absorb Sr and Ca metabolically has only been demonstrated in the absence of competing
* This report is based on work performed under Contract AT-(04-3)-34, PA 23 with the United States Atomic Energy Commission. 273
274
R. HANDLEY and K. L. BABCOCK
ions. For this reason a new study of Sr uptake and translocation by maize was undertaken with emphasis upon the influence of other ions upon metabolic and non-metabolic uptake by excised roots and the relation of these effects to the upward translocation of Sr in intact plants. The interfering ions selected were Ca, because of its chemical similarity to Sr, and K which M.A~(17) has demonstrated to inhibit Ca uptake by excised maize roots. MATERIALS A N D M E T H O D S
The excised-root material was obtained by germinating maize seed (yea mays L. var. Golden Cross Bantam) in running tap water overnight and subsequently supporting it on open-weave cheesecloth over an aerated solution 0.1 m M in Ca(NO3)z, K H 2 P O 4 and M g S O 4 for 5 days at 26°C in darkness. A 4-I. beaker was used for 100 seeds, the liquid level being about 1 cm below the cloth. A polyethylene bag used as a cover to maintain a humid atmosphere was removed on the third day. The roots of 200 plants were excised on the fifth day at the seed and segments about 1 cm long were cut into 2 liters of water. After mixing, the root material was filtered off on a sieve of cotton towelling, washed with 3 liters of water and finally freed of excess water by applying vacuum. Samples of 1.00 g fresh weight were used with a solution "volume of 1-0 1. Root samples were separated from the experimental solutions using W h a t m a n No. 541 paper and vacuum. Before analysis the samples were rinsed with water, dried at 60°C and weighed. Sr uptake was determined using SrCI~ solutions (0.005 N) labelled with 85Sr (4.0 ~Ci per liter) and standard techniques. K and Ca were determined by absorption spectroscopy after ashing and solution of the ash. Except where otherwise indicated all figures presented represent averages of 3 or more determinations. For the experiment with whole plants, maize seed was germinated and grown for 3 days in dilute culture solution as described above. T h e n 54 seedlings with roots about 10 cm long were transplanted into 1/10 strength Hoagland solution. T h e plants were supported on perforated lids made of wax-impregnated plaster of Paris resting on white plastic flower pots (J. M.
McConkey Inc. Puyallup, Washington) of about 3-1. capacity. Each of 18 pots held 3 plants. The pots were wrapped with aluminum foil to exclude light. The experiment was carried out after the plants had grown thus in the greenhouse with aeration for 2 weeks. At that time the dilute culture solution in each pot was replaced by the appropriate experimental solution after thorough washing of pots and roots in running water. T h e SrCI~. solutions were 0.005 N. T h e KCI and CaC12 solutions were 0.001 N. All solutions were labelled with 20 [zCi of SsSr per liter and were aerated. T h e total volume in each pot was 2.5 1. After 24 hr and after 40 hr the plants in 9 pots were harvested. The roots were washed in running distilled water and the plants were separated into root and shoot fractions. These were dried for several days at 60°C, weighed and then ground using a Wiley mill and the 20 mesh screen. Weighed samples were then counted using a well-type scintillation detector (Tracerlab Model SC-54) and a g a m m a spectrometer (Tracerlab Model SC-78) with a window width of 2.0 V. The standards consisted of 2"00 ml samples of the well-stirred experimental solutions taken just prior to introduction of the plants. The plants taken for analysis at both sampling times were healthy in appearance with no evidence of injury. RESULTS AND DISCUSSION
Uptake of Sr by excised roots over a 5-hr period at 26°C and at I°C is shown in Fig. 1. The amounts of Sr absorbed by this material were much less than those found in earlier workCn) where newly vacuolated tissue close to the root apex absorbed about 30 mequiv per kg fresh weight in 5 hr at 26°C. T h e corresponding figure for the whole root used in these experiments was only about 7.5 mequiv per kg. This was to be expected since the material used here was overwhelmingly composed of mature cells which are well known to be less active in salt uptake than those immediately proximal to root meristems. T h e amounts absorbed at 26°C were only slightly less than those reported by M,~m(17) for Ca uptake by 6-cm apical segments of maize roots of the deKalb variety but the uptake of Sr at low temperature was greater and at 5 hr amounted to 60 per cent of that taken up at 26°C.
UPTAKE AND TRANSLOCATION OF Sr BY ZEA MAI'i~
275
5oL o
5O
u3
0
I
I
I
l
]
~
2
3
4
5
Time tn hours
FIO. 1. Uptake of Sr by root segments of maize from 0.005 N SrCI2 at 26°C and at I°C (lower curve). Thus although a pronounced temperature effect was found with segments representing the whole root a relatively large non-metabolic component was indicated. At 5 hr in the cold the tissue was not yet in a steady state with the external solution. Sr entry was continuing albeit at a slow rate. This strongly suggests passage through a barrier presumably the plasmalemma which limxts the rate of entry. T h e curve presented by M~t~ts(17) for Ca uptake at low temperature is similar in this respect. It is possible of course that imposition of a low temperature alters the permeability of the plasmalemma but the ability of plants such as barley, OS) for which no metabolic uptake of Ca can be demonstrated in excised roots, to transport Ca to the shoot argues that the plasmalemma is normally permeable to alkaline earth cations. U p w a r d transport implies entry into the symplasm. (2,s) Uptake of Sr at 1°C is accompanied by loss of native K. K loss represents about 80 per cent of the Sr taken up in 5 hr. No loss of native Ca occurs. At 26°C no loss of either K or Ca was detected. Possibly at the higher temperature K displaced from cell wall and cytoplasmic binding sites is metabolically sequestered in vacuoles rather than being released to the solution. T h e design of these experiments does not
permit any evaluation of the amounts of Sr which m a y be lost from the cut ends of the root segments after absorption. At l°C these are probably close to nil since several studies( 4, s, 7,1416,10) have shown release of ions into the xylem to be under metabolic control. Therefore while the curve shown in Fig. 1 for uptake at I°C probably represents passive uptake accurately, the amounts of Sr absorbed indicated for various times at the higher temperature m a y be erroneously low. There appears to be no simple way to eliminate this possible error. Use of longer root segments or even whole roots cut only at the seed would not eliminate it since the data of EVANS(7) indicate that the amounts of Ca exuded by maize-root sections are a linear function of the segment length exposed to the solution containing Ca. Solution of this problem will require experiments designed to measure both uptake and exudation. Methods for this purpose have been designed by EvANs(7) and by MooRE et al.(10) but apparently have not been extensively used as yet. The data of Table 1 indicate that a large fraction of the labelled Sr taken up at 26°C is resistant to removal by unlabelled SrC12 solutions. For these experiments the root samples were allowed to take up Sr from SrC12 solutions
276
R. HANDLEY and K. L. BABCOCK Table 1. Lossfrom excised roots of absorbed Sr labelled with s6Sr to unlabeUedSrClz*
Sr, ~tequiv/g, dry wtq-S Before After elution elution
Uptake solution
Elution temperature
Sr*CI2 0.005 N
26°C
144+7
84+5
58
Sr*C12 0.005 N
I°C
144+7
94::k6
65
Sr*C19. 0.005 N + CaCI~ 0:001 N
26°C
118+9
70+5
59
Sr*C19. 0"005 N + CaC19. 0.001 N
I°C
118+9
69+4
59
% retention
* 5-hr absorption period, 5-hr elution period. labelled with SSSr for 5 hr and were then transferred after brief rinsing for a further 5 hr to urdabelled solutions of the same concentration (0-005 N). About 60 per cent of the Sr taken up remained with the tissue after elution. This indicates a site of Sr accumulation deeper in the cell than the plasmalemma since this m e m b r a n e appears permeable to Sr. This site is probably at the tonoplast since previous work(10-a2) has shown accumulation of Na, Ca and Sr by maize roots to occur coincidentally with the appearance of well-defined (i.e. membranelimited) vacuoles. Whether or not the plasm a l e m m a is also active in Sr accumulation is not apparent. Note that the concentration of Sr (0.005 N) used in these experiments is well above that at which the first or high-affinity mechanism described by EPSTEIN(5,e) for the uptake of monovalent ions becomes saturated. This mechanism m a y exist at the plasmalemma. The data of MnAst 17) indicate such a mechanism to be operative in Ca uptake by maize roots. However the resistance to elution of Ca absorbed from solutions of very low concentration (0.010.2 mequiv per 1.) was not reported. T h e data of Table 1 and Fig. I indicate that
the concentration of labile Sr (i.e. presumably that physically bound on cell walls and in the cytoplasm) is lower when operation of the vacuolar uptake mechanism is permitted. While the 5-hr uptake at I°C is 60 per cent of that taking place at 26°C (Fig. 1), only about 40 per cent of the Sr taken up at 26°C is readily elutable. Subtraction of the uptake at I°C from that at 26°C would in this case yield an erroneously low estimate of the metabolically absorbed fraction. Losses of Sr via xylem exudation as well as sequestration of Sr in the vacuoles probably contributes to this effect. Penetration of the plasmalemma appears to be the rate-limiting step in Sr uptake at this concentration. T h e effects of increasing K concentrations upon the 5-hr uptake of Sr at 26°C and at I°C are shown in Fig. 2. At 26°C relatively low concentrations of K inhibit Sr uptake strongly. Addition of 1.0 mequiv per 1. of K to the 0'005 N SrC12 solution (equivalent per cent K = 1 6 . 7 ) caused a 40 per cent reduction in Sr uptake. At higher concentrations of K a linear relationship between Sr uptake and K concentration obtains. With metabolism suppressed by lowering the temperature to I°C the effect
UPTAKE AND TRANSLOCATION OF Sr BY ZEA I14AYS
277
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g "5
75
c
o.
5O
25
I
0
15
I 30
I
I
I
45
60
75
Equivolent percenl K in solulion
FIO. 2. Effect of K on the 5-hr uptake of Sr by root segments of maize at l°C and at 26°C (lower curve). Sr concentration 0.005 N. of K is greatly reduced and the relationship is linear over the range of K concentration used. It appears that at relative K concentrations above about 25 per cent the metabolic phase of Sr uptake is virtually elilrfinated and that further additions of K are solely effective in reducing the non-metabolic phase by competition for cytoplasmic and cell-wall binding sites. Note that the linear portion of the graph obtained at 26°C parallels the straight line obtained for K interference at 1°C. T h e data of Fig. 2 suggest that the metabolic process responsible for Sr accumulation is the same as that for K and that K is greatly preferred over Sr. The results obtained by MAAS(17) for Ca uptake by maize roots indicate that the same mechanism also accepts Ca. However, with maize roots as with the excised roots of other plants Sr and Ca exert stimulatory rather than inhibitory effects upon K uptake (Table 2, 9) and it is apparent that more than simple competition for a common carrier is involved. It m a y be that Sr inhibits the transfer of K to the xylem and so its loss to the solution via the cut ends of the root segments. We have observed that the presence of Ca in the medium very strongly inhibits Cs transloeation to the shoot of maize. T h e interaction of Sr and K in this regard would be expected to be similar. These data have not been published as yet.
Table 2. Effect of Sr on K uptakefrom 0"005 N KCl
Sr, mequiv per 1.
Sr, equiv %
0 1.0 3.0 5.0 7.0 10.0
0 16"7 37.5 50-0 58.4 66"5
K uptake, tzequiv]g K uptake, (dry)* % of control 232 247 259 274 289 284
100 106 112 118 124 122
* Average value, 2 determinations. The effects of increasing concentrations of Ca upon Sr uptake at 26°C and at I°C are shown in Fig. 3. Unlike K, Ca inhibited Sr uptake more effectively at I°C than at 26°C. Indeed, concentrations of Ca up to about 10 equivalent per cent had no significant effect upon Sr uptake at 26°C. Above this level Sr uptake declined linearly with Ca concentration. At 1°C a linear relationship obtained over the range of Ca concentrations tested. T h e total effect of Ca upon Sr uptake by excised roots thus appears to involve both stimulatory and inhibitory factors. T h e inhibitory factor is exerted principally at least upon the non-metabolic phase of Sr uptake through competition for adsorption
278
R. HANDLEY and K. L. BABCOCK
t00
E 75
o. 50
25
I t0
0
I 20 Equ~volenl
percent
I 30
I 40
I 50
Co in s o l u t i o n
FIO. 3. Effect of Ca on the 5-hr uptake of Sr by root segments of maize at 26°C and at I°C (lower curve). Sr concentration 0.005 N. sites. Note that the straight-line portions of the graphs obtained at 26°C and at 1°C are nearly parallel. The stimulatory factor which, at low relative concentrations of Ca, is able to negate this inhibition does not appear to be exerted at the tonoplast. The presence of Ca in the medium had no effect upon the retention of absorbed labelled Sr by excised root segments against elution by an unlabelled solution (Table 1). That is, the presence of Ca did not affect the distribution of Sr between the labile phase and the sequestered phase which we postulate to
reside in the vacuole. Rather it appears to be exerted upon the metabolic transfer of Sr to the xylem. The experiments with whole plants described below tend to support this interpretation. The implications of Figs. 2 and 3 are perhaps somewhat more clearly evident in the data shown in Table 3. To obtain these data the 3-hr and 5-hr uptake of Sr from 0.005 N SrC12 was measured using the pure solution and solutions containing 1"0 mequiv of CaC1,. or KC1 per liter. Measurements were made at I°C and at 26°C. The data indicate that at
Table 3. Effects of Ca and K on Sr uptake by excised rootsfrom 0.005 aV SrCI~
Expt. no.
Time, hr
Interfering ion*
5 5 6 6 7 7 8 8
5 5 3 3 5 5 3 3
None Ca None Ca None K None K
* Interfering ion cone. = 1.0 mequiv/1.
26°C
I°C
Uptake at 26°C, % of control
134.0-t-4.9 121.1 4-0.9 104.5 4-1.9 90.64-0.7 130.0-t-2.5 80.5-4-1.7 116"8:tz3.4 71"2 -t-2.8
79"4-t-0.8 66.7 4- 1.0 72"1 4-1-7 59.9 4-0.9 84.54-1.6 79.9 4- 0.5 70.3 4-0"3 70-6 4-1.1
100 90.4 100 86.7 100 61-7 100 60"9
Av. Sr uptake izequiv/g, dry wt 4- S
Uptake at I°C, % of control I00 84.0 100 83.1 100 94.6 100 100.4
UPTAKE AND TRANSLOCATION OF Sr BY ZEA MA ]':S' the concentrations of Sr and interfering ions used the inhibitory effect of K is exerted almost entirely upon the metabolically mediated phase of Sr uptake and that of C,a upon the nonmetabolic phase. Note that, although the total inhibitory effect of Ca (i.e. the effect at 26°C) is much less than that of K, the ability of Ca to reduce the non-metabolic phase exceeds that of K. This is of course to be expected in view of the higher adsorption energy of the divalent ion. Ca appears to be only weakly competitive with Sr for metabolic uptake. Note however that the competitive ability of Ca at the tonoplast would be partially masked if, as postulated above, Ca exerts an inhibitory effect upon transfer of Sr to the xylem. The effects of K and Ca on the uptake and distribution of Sr by whole maize plants are seen in Table 4. Two effects of K are evident: (1) a reduced total uptake and (2) a pronounced reduction of the root-shoot concentration ratio. The data obtained with excised roots would lead one to expect a sharply reduced Sr uptake by the
279
root when K is present in the medium. However if the inhibitory effect of K were exerted at the tonoplast only, reduction of the amount of Sr found in the shoot would not be expected. The resistance of metabolically absorbed (i.e. vacuolar) Sr to elution shown above (Table 1) suggests that Sr sequestered in vacuoles of the root cortex is only very slowly available for upward transport. In view of the reduced concentrations of Sr found in the shoots of plants receiving K it appears most likely that K also interferes with the metabolically controlled mechanism responsible for the pumping of Sr into the xylem. The location as well as the identity of this mechanism is unknown at present. The endodermis,( TM the young xylem cells themselves(1,1s) and the stelar parenchyma(5,1s,le) have been suggested as the active sites. The lowered root-shoot concentration ratios for Sr absorbed from solutions containing K and indeed the failure of K to suppress entirely the upward movement of Sr indicate that K is much less effective here than at the tonoplast in inhibiting Sr secretion.
Table 4. Effect of K and Ca on uptake and root-shoot distribution of Sr
Interfering ion
Plant fraction
Dry wt, g
None
Root Shoot Root Shoot Root Shoot Root Shoot Root Shoot Root Shoot Root Shoot Root Shoot Root Shoot
0.345 0.970 0.356 0.901 0.408 1.049 0.546 1.418 0.411 1.085 0.291 0.840 0.440 1"215 0.440 0.949 0-361 1.029
None None K K K Ca Ca Ca
Sr~ [zequiv Sr, in conc. [xequiv]g fraction 585 124 595 133 604 130 234 87 229 81 220 74 538 99 541 108 591 92
202 120 212 120 246 136
128 123 94 88 64 62 237 120 238 103 213 95
Sr, % in root
Sr, cone. ratio root]shoot Av.4-S
St, cone. whole plant ~equiv/g Av.+S
Sr, cone. whole plant % cont.
4.6±0.1
2574-11
100
2.84-0-2
1204- 9
47
5-64-0.7
2284-16
89
63 64 64 51 52 51 66 70 69
280
R. HANDLEY mad K. L. BABCOCK
We have the feeling, but at present no data to support it, that the relative inefficiency of K in this regard may be related to the preferential absorption of K by phloem tissue. This would reduce the effective concentxation of K in the vicinity of the xylem. K is moved readily in the phloem whereas Ca and Sr are largely excluded.CS) The presence of Ca, predictably in view of the results obtained with excised roots, had a smaller effect than K upon total uptake but lowered both root and shoot concentrations. The principal effect of Ca was to reduce the root-shoot translocation of Sr. The concentration of Sr in the root was lowered (as with excised roots) only about 6 per cent by the presence of Ca in the medium amounting to 16.7 per cent of the cation concentration while the Sr concentration in the shoot was lowered by 22 per cent. This suggests that the failure of relatively low concentrations of Ca to inhibit Sr uptake by excised roots at 26°C (Fig. 3) was due to a reduction in the ability of roots receiving Ca to pump Sr into the xylem. I n experiments with excised roots this effect would of course counter the inhibitory effect of Ca. As mentioned above we have found a similar though much more marked effect of Ca with respect to Cs translocation in maize. The same phenomenon was noted by JACKSONet al.~14) who reported the effects of various cations on the uptake and translocation of Cs by wheat seedlings. It would appear from this that the Viets effect,~*°) i.e. the stimulation of K, Rb and Cs uptake by Ca and other polyvalent ions by excised roots may be exerted at the stele rather than at the cell membranes or tonoplasts of the cortical cells. The data of Table 4 represent the results obtained using a 24-hr absorption period. A similar experiment using a 40-hr period yielded closely similar results. In the interest of economy these results are not presented here. The results of this work indicate that the high degree of Sr mobility with respect to root-shoot transport found for maize in the previous experiments(S) was due to 3 factors: (1) the relatively large non-metabolic component involved in Sr uptake, (2) the effect of K in reducing or eliminating Sr sequestration in vacuoles of the root cortex and (3) the relatively
smaller effects of K and Ca in inhibiting Sr uptake into the xylem. The effect of K in reducing vacuolar uptake is of particular importance in this regard since in the presence of K the ability of the maize root to sequester Sr is largely eliminated so that it behaves much as do the roots of other plants lacking this ability.
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2. 3.
4.
5. 6.
7. 8.
correlation between structure and function in the root of Zea mays. J. Exptl Botany 18, 544-555. ARISZW. H. (1956) Significance of the symplasm theory for transport across the root. Protoplasma 46, 1-62. BnRBERD. A. and KOONTZH. V. (1963) Uptake of dinitrophenol and its effect on transpiration and calcium accumulation in barley seedlings. Plant Physiol. 38, 60-65. DREW M. C. and BmDULPHO. (1971) Effect of metabolic inhibitors and temperature on uptake and translocation of 45Ca and 42K by intact bean plants. Plant Physiol. 48, 426-432. EPSTEXN E. (1971) The upward movement of water and nutrients, pp. 151-189. In, Mineral nutrition of plants. Wiley, New York. EPSTEINE., R~INSD. W. and ELZAMO. E. (1963) Resolution of dual mechanisms of potassium absorption by barley roots. Proc. Natl Acad. Sci. 49, 684-692. EvANsE. C. III (1964) Polar transport of calcium in the primary root of Zea mays. Science 144, 174-177. I-~NDLEYR. and BABOCKK. L. (1972) Translocation of 85Sr, 137Cs and l°SRu in crop plants. Radiation Botany 12, 113-119.
9. HANDLEY R., MJ~TWALLY A. and OVERSTREET R.
10. 11. 12.
13.
(1965) Effects of Ca upon metabolic and nonmetabolic uptake of Na and Rb by root segments of yea mays. Plant Physiol. 16, 513-520. HANDLEY, R. and OV~RSTR~ET R. (1961) Uptake of calcium and chlorine in roots of yea mays. Plant Physiol. 36, 766-769. HnNDLEYR. and OV~RSTREETR. (1963) Uptake of strontium by roots of Zea mays. Plant Physiol. 38, 180-184. HAbrDLEYR., VmAJ. R. D. and OVERSTR.EETR. (1960) Metabolic and non-metabolic uptake of sodium in roots of Zea mays. Plant Physiol. 35, 907-912. HYLMOB. (1953) Transpiration and ion absorption. Physiol. Plantarum 6, 333-405.
UPTAKE AND TRANSLOCATION OF Sr BY ZEA zl~IAYS 14. JACKSONW. A., Luco H. M. and CRAIGD. (1966) Cesium uptake from dilute solutions by young wheat seedlings as affected by selected cations. Plant Soil 24, 33-53. 15. L.~UCHLI A. and EPSTEIN E. (] 971) Lateral transport of ions into the xylem of corn roots I. Kinetics and energetics. Plant Physiol. 48~ 111-117. 16. LXucrILI A., SPURR A. R. and EPSTEIN E. (1971) Lateral transport of ions into the xylem of corn roots II. Evaluation of a stelar pump. Plalzt Physiol. 48, 118-124.
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17. MAAS E. V. (1969) Calcium uptake by excised maize roots and interactions with alkali cations. Plant Physiol. 44, 985-989. 18. MOORE D. P., JACOBSON L. and OVERSTm~.ETR. (1961) Uptake of calcium by excised barley roots. Plant Physiol. 36, 53-57. 19. MOORED. P., MASONB.J. and MARSE. V. (1965) Accumulation of calcium in exudate of individual barley roots. Plant Physiol. 441,641-644. 20. VIETSF. G. (1944) Calcium and other polyvalent ions as accelerators of ion accumulation by excised barley roots. Plant Physiol. 19, 466-480.