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Translocation of carrier-free 85Sr, 137Cs and 106Ru in woody plants
Radiation Botany, 1970, Vol. 10, pp. 577 to 583. Pergamon Press. Printed in Great Britain.
T R A N S L O C A T I O N OF C A R R I E R - F R E E S~Sr, ~ C s AND ~°6Ru IN WOODY PLANTS* R. H A N D L E Y a n 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 8 oTune 1970) A b s t r l c t - - C a r r i e r - f r e e solutions of t87Cs and t°eRu were applied to the foliage of three genera of woody shrubs (Ceanothus, Adenostoma and Quercus) and subsequent translocation into untreated portions of the plants was measured. In all cases the bulk of the retained dose remained with the directly treated material. The results indicate that in these genera foliarly applied x3~Cs is no more mobile than Sr while X°6Ru is considerably less mobile than either. In another series of experiments the distribution of 8~Sr, xn~Cs and X°3Ru between the root, the old growth and the new growth was determined after incorporation of the isotopes into Ceanothus and Adenostoma via their root systems, xsvCs and especially X°eRu were largely retained in the root. A relatively large fraction of the retained dose of SSSr was found in the shoot. In both series of experiments a preferential movement of xS~Cs into new growth was observed. R~mmmg---On a appliqud des solutions de 137Cs et ~°eRu sans entraineur au feuillage de trois genres de plantes ligneuses fourrag6res (Ceanothus, Adenostoma et Quercus). On a ensuite mesur~ leur translocation dans les portions des plantes non traitdes. Dans tousles cas, la majeure partie de la dose retenue reste avec le materiel directement traitS. Les r~ultats indiquent que, dans ces genres, le 13~Cs appliqud au feuillage n'est pas plus mobile que Sr alors que l°eRu est beaucoup moins mobile que l'un ou l'autre isotope. Dans une autre s~rie exp~rimentale, la distribution de ssSr, 137Cs et l°6Ru parmi les vieilles et les nouvelles pousses et les racines &ait d&ermin~e a p r ~ incorporation des isotopes h Ceanothuset Adenostomapar leur syst6me radiculaire. ~sTCs et spdcialement ~°eRu sont fortement retenus par la racine. Une fraction relativement importante de la dose de esSr retenue se retrouve dam le rejeton. Dam les deux s~ries d'exp~rience, on retrouve un mouvement pr~f~rentiel du ~37Cs dans les nouvelles pousses. Z u s a m m e n f a s s u n g - - D a s Blattwerk von drei Arten holziger Futterpflanzen (Ceanothus, Adenostoma und Quercus) wurden mit tr~igerfreien L6sungen yon 137Cs und t°6Ru behandelt und anschliessende Translokation in unbehandelte Teile der Pflanzen wurde gemessen. In allen F~illen blieb der gr6sste Teil der erhaltenen Dosen im direkt behandelten Material. Die Ergebnisse zeigen, dass fiir die Bl/itter dieser Arten angewandte t3~Cs nicht beweglicher ist als Sr, w/ihrend ~°6Ru betr~ichtlich weniger beweglich ist als beide. In einer anderen Reihe yon Experimenten wurde die Verteilung yon S6Sr, xs~Cs und X°6Ru zwischen Wurzel, altem und neuem Wachstum nach der Inkorporation der Isotopen in Ceanothus und Adenostoma durch ihr Wuzelsystem bestimmt. ~37Csund besonders X°nRuwurden weitgehend in der Wurzel zuriickbehalten. Ein verh~iltnism~issig grosser Teil der zuriickbehaltenen Dosis von ~Sr wurde in der Sch6sslingsspitze gefunden. Bei beiden Versuchsreihen wurde eine bevorzugte Bewegung des IS~Csin das neue Wachstum beobachtet. *This report is based on work performed under Contract AT-( 11-1 ) with the United States Atomic Energy Commission. 577
R. HANDLEY and K. L. BABCOCK
578 INTRODUCTION
THE RESULTS of experiments dealing with the translocation of sSSr in 3 genera of xerophytic shrubs eaten by browsing animals were reported previously.(5) In these experiments carrier-free solutions of SSSr were applied to selected portions of the foliage ofCeanothus, Adenostoma and Quercus plants following which movement of the isotope into new growth and other untreated portions of the shoot was measured. The data obtained indicate that Sr is considerably more mobile in Ceanothus and Adenostoma than it has been shown to be in a variety of crop plants. (~,9.,e, s-10) Under field conditions where the plants were subject to occasional wetting, about 6 per cent of the retained dose was found in growth which occurred during the three-month interval between treatment and harvest. The m a x i m u m amounts of s 5Sr translocated from bean and corn leaves (also rewetted periodically during the experiment) were reported by Ambler to be 0.6 and 0"5 per cent of the applied dose respectively.(1) The reason for this difference in behavior is presently unknown. It is the more remarkable since in our experiments with woody shrubs much of the dose was applied to the outer bark rather than being confined to the leaves. Thus it seems likely that an undetermined part of the applied dose was not available for absorption and redistribution. Were it possible to estimate that portion and subtract it from the total dose administered, an even larger translocated percentage would of course be computed. Also, because of the greater development of the leaf cuticle in xerophytic plants such as Ceanothus and Adenostoma absorption and redistribution of ions applied to the leaves would perhaps be expected to be more restricted than in mesophytic crop plants. It is possible however that the failure of mesophytic plants to translocate foliarly applied Sr more readily may not be due primarily to the inability of Sr to penetrate the leaf cuticle, but rather to the active absorption and sequestration of-Sr by the leaf tissue. Levi has presented data suggesting that active accumulation of 134Cs by bean leaves limits translocafion of this isotope.(v) In view of the results obtained in our earlier experiments it became of interest to know to what extent the ability of Ceanothus and Adenostoma to translocate foliarly applied Sr extended to other
fallout components. To investigate this, similar experiments have been done using carrier-free lsTCs and l°6Ru. Translocafion offoliarly applied x37Cs and 134Cs has previously been studied in beans and other crop plants.0,e-o) In these studies Cs has been shown to be more readily absorbed and translocated than Sr. Thus in the experiments conducted by MIDDLETON(8) less than 0.5 per cent of the applied dose of sgSr was found in the tubers of potato plants after foliar contamination whereas 25-30 per cent of the dose was found in the tubers after foliar contamination with 13~Cs. The data presented by KLECHKOVSKY and GULIAKIN(6)indicate that in sunflower and bean l°eRu like °°Sr is not readily translocated from contaminated leaves. The results obtained in the experiments involving foliar applications of ssSr, ls~Cs and ~°6Ru to Ceanothus and Adenostoma suggested that the rate limiting step in absorption and translocation might be the initial penetration of the leaf cuticle. To investigate this the relative mobilities of S~Sr, 137Cs and X°eRu were determined by measuring their movement into new growth after incorporating the isotopes into the plants via the root system rather than the foliage. MATERIALS
AND METHODS
For the experiments involving foliar applications of isotopes the methods were similar to those previously reported.~5) Small specimens of Ceanothus cuneatus, Hook. (Buck Brush), Adenostoma fasciculaturn, H. and A. (Chamise) and Quercus durnosa, Nutt. (Scrub Oak) were transplanted at the Hopland Field Station of the University of California into one-gallon cans and allowed to become well established over a period of several months. In the spring, just prior to the onset of new growth the plants were placed in the greenhouse at Berkeley. Six plants of each species were treated with lSVCs, six with l°6Ru. This was done by painting selected parts of the foliage with carrier-free solutions of laTCsC1 or l°eRuCl3 containing 10~.c per ml. Because the isotopes were received in dilute HCI the diluted solutions used were slightly acid. Neutralization was not deemed desirable because of the effects upon uptake which might have been produced by the introduction of a competing ion. The painted plants became dry within a few minutes
TRANSLOCATION OF CARRIER-FREE ssSr, xaTCs AND X°6Ru IN WOODY PLANTS and no evidence of injury to the treated portions was observed. Removal of HC1 from the solutions by evaporation was not feasible because both ~37Cs and l°eRu are tenaciously held by the walls of containers. After taking carrier-free solutions to dryness large fractions of the activity cannot be redissolved in water. Following treatment and marking of growing points with India ink the cans (perforated at the bottom) were placed in shallow containers (2 in. high) which were kept filled with water. This method of irrigation reduced the danger of wetting the shoots. After 8 weeks the whole aerial portion of each plant of Ceanothus and Adenostoma was separated into 4 fractions: new growth on untreated branches, untreated old growth, new growth on treated branches and treated old growth. The Quercus specimens were very small. For this reason it was practicable in this case to separate only treated old growth and new growth on treated branches. The various fractions were dried at 70°C, ground in an intermediate Wiley mill to pass the 20 M screen and their content of ~87Cs or ~°eRu determined by measuring the g a m m a emission of weighed samples. For study of the translocation of SSSr, x37Cs and l°eRu introduced into the plants via the roots, small specimens of CeanothusandAdenostoma obtained at the Hopland Field Station were transplanted into 4 1. beakers containing I/4 strength Hoagland solution. The roots were washed free of adhering soil before transplanting. The plants were maintained with continuous aeration for two weeks in a lath house. T h e y were protected from rain by means of a shelter made of polyethylene sheeting. This was carried out in February of 1969. The lath house was used rather than a greenhouse because the greater warmth of the latter would have induced the onset of new growth prematurely. After two weeks isotopes were added as carrier-free solutions to the beakers. Three plants of each genus were treated with each isotope. The initial concentrations of isotopes in the nutrient media were as follows: ssSr, 13.9 ~tc/1; l°eRu, 18"7 ~tc/1 and laTCs, 14.3 ~tc/1. The p H was about 5.5. The plants were allowed to remain in the radioactive solutions for one month, at the end of which the beginning of new shoot growth was apparent. The roots were then washed with five 41. changes
579
of 0.01 N CaCI 2 and the plants were transplanted into non-radioactive 1/2 strength Hoagland solutions. At this time the growing points of each plant were marked with India ink and all plants were removed to the greenhouse in order to promote more rapid growth. After 5 weeks each plant was cut into 3 fractions representing old shoot growth, new shoot growth and total root. The fractions were dried, ground and analyzed as described above. Some confusion m a y be occasioned by the use of the term "dose". In this paper (as in m a n y others) this word designates a quantity of a radionuclide measured in microcuries. The same word is of course also in general usage to mean radiant energy absorbed per g.
RESULTS AND DISCUSSION
The results of experiments with foliarly applied 13~Cs are presented in Tables 1 and 2. It is apparent that as in the earlier experiments with 85Sr¢5) the bulk of the laTCs applied remained with the directly treated material, over 98 per cent of the retained dose being found in this fraction of all 3 genera. In Ceanothus 1-6 per cent of the laTCs retained was found distributed among the untreated fractions after 8 weeks. The corresponding figure for ssSr(S) was 3"2 per cent. In Ceanothus the mobility of 85Sr thus apparently exceeds that ofl37Cs. In Adenostoma the mobilities measured in this way were about equal while in Quercus the mobility of 137Cs was slightly greater than that of SSSr. These results are strikingly different to those obtained by MIDDLEToN(S, 9) and othersll,2,6,1°) which indicate that in potatoes and other crop plants foliarly applied carrier-free Sr is virtually immobile while 137Cs is readily translocated from the site of contamination. Although in Ceanothus and Adenostoma the amounts of 137Cs and ssSr translocated (expressed as per cent of the retained dose) are similar the distributions of the two isotopes within the untreated material are quite different. This is apparent in the data of Table 2. The tendency of 137Cs to accumulate in younger or actively growing tissue is well expressed in both Ceanothus and Adenostoma. 85Sr tended to move acropetally into contiguous new growth and basipetally into untreated old growth in about
R. HANDLEY and K. L. BABCOCK
580
Table 1. Translocation of 127Cs applied to thefoliage of woodyforage plants Dry wt., g
laTCs cone., ~tCi/g
x37Cs total in fraction, btCi
12'Cs, % of retained dose ± S
(a) Ceanothus I. Old growth, treated 2. Old growth, untreated 3. New growth, treated branches 4. New growth, untreated branches
6.24 5.62 0.78 0.57
4"21 -+ 102 0'97 37"64 2'00
21"97 × 102 5"18 25.59 1"04
98.41 _+ 1.13 0.32 _+0.28 1.29 + 0.82 0.04-+ 0.03
(b) Adenostoma 1. Old growth, treated 2. Old growth, untreated 3. New growth, treated branches 4. New growth, untreated branches
2.91 1-72 0.94 0.69
4"78 x lOs 1.52 10"91 1.58
10"91 × lOs 2'92 11"88 0"96
99.00 _+0.92 0.20_+0.18 0.88 _+0.65 0.06 _+0.04
(c) Quercus 1. Old growth, treated 2. New growth, treated branches
0.49 0.35
9.15 x 102 16.29
3.94× 102 4.33
98.34_+2.18 1.24_+ 1.02
Plant fraction
Table 2. Distribution of translocated ssSr, 13~Csand *°SRu after foliar contamination % of translocated dose x87Cs lO6Ru
Plant fraction
ssSr
(a) Ceanothus 1. Old growth, untreated 2. New growth, treated branches 3. New growth, untreated branches
50.0 46.8 3.2
16.3 80.6 3.3
61.6 31.9 8.0
(b) Adenostoma 1. Old growth, untreated 2. New growth, treated branches 3. New growth, untreated branches
58.0 34.5 7.6
18.5 75.4 6.1
47.4 39.1 13.5
equal amounts.(5) M o v e m e n t o f 137Cs was pred o m i n a n t l y into the new growth, 80.6 a n d 75.4 p e r cent o f the translocated 13~Cs being found in this fraction of Ceanothus a n d Adenostoma respectively. Note also ( T a b l e 1) t h a t the conc e n t r a t i o n oflSTCs in the new g r o w t h o f u n t r e a t e d branches exceeds t h a t in the old growth. T h e d a t a suggest t h a t while foliarly a b s o r b e d Sr is distributed b y diffusion a n d convectively in the t r a n s p i r a t i o n stream, the distribution o f Cs m a y involve in p a r t a m e t a b o l i c a l l y m e d i a t e d transp o r t process w h i c h concentrates this ion in actively g r o w i n g tissue. T h e translocation o f
foliarly a p p l i e d 137Cs b y p o t a t o plants to d e v e l o p i n g tubers r a t h e r t h a n solely to transp i r i n g parts of the plants has been n o t e d b y MIDDLETON. (s, 9) O n l y a v e r y slight t r a n s l o c a t i o n o f X°SRu o c c u r r e d in all three g e n e r a with no evidence of preferential m o v e m e n t into new g r o w t h ( T a b l e 3). This is in accord w i t h the low m o b i l i t y of l°SRu a p p l i e d to the leaves of b e a n a n d sunflower r e p o r t e d b y KLECHKOVSKY a n d G U L I A K I N . (e)
T h e d a t a o b t a i n e d i n d i c a t e the following o r d e r o f m o b i l i t y with respect to foliar a p p l i c a t i o n :
T R A N S L O C A T I O N OF C A R R I E R - F R E E ssSr, 187Cs AND X°6Ru IN W O O D Y PLANTS
581
Table 3. Transloeation of l°6Ru applied to thefoliage of woodyforage plants Dry wt., g
X°SRu cone., ~tCi/g
X°6Ru, total in fraction, ~tCi
i°6Ru, % of retained dose _+S
(a) Ceanothus 1. Old growth, treated 2. Old growth, untreated 3. New growth, treated branches 4. New growth, untreated branches
5.48 4.52 0.51 0.88
5.96 x 102 0.53 2-73 0.49
25.47 x 10 ~ 2.47 1.31 0.33
99.90 + 0.16 0. i 1 + 0.068 0"09 + 0-13 0.01 + 0.007
(b) Adenostoma 1. Old growth, treated 2. Old growth, untreated 3. New growth, treated branches 4. New growth, untreated branches
3.68 2.09 1.30 0.90
5.40 × 10 ~ 0.65 0.65 0.35
19.26 x 102 1.20 0.99 0.34
99.86 + 0-06 0-07 + 0.05 0.08 + 0.08 0.05 + 0.14
(c) Quercus 1. Old growth, treated 2. New growth, treated branches
0.61 0.52
10.04 × 102 0.09
4.83 × I02 0.06
NI00 < 0.01
Plant fraction
S r . ~ C s > ~ R u . I n view of the relatively high m o b i l i t y o f f o l i a r l y a p p l i e d Cs r e p o r t e d for mesop h y t i c plants, the results o b t a i n e d here suggest t h a t in Ceanothus a n d Adenostoma the a p p a r e n t mobilities o f these ions m a y reflect largely the rates at w h i c h they p e n e t r a t e the l e a f cuticle a n d in t u r n their b i n d i n g energies at the leaf surface. Cs is k n o w n to be a d s o r b e d m u c h m o r e strongly than Sr b o t h to soil colloids(X2,13) a n d to p l a n t tissue33, 4) T h e failure of foliarly a p p l i e d xzTCs to be t r a n s l o c a t e d as r e a d i l y as it is in crop plants m a y reflect differences in the composition or structure of the l e a f cuticle in xerophytes as comp a r e d to mesophytic plants. T h e b e h a v i o r of X°eRu with respect to a d s o r p t i o n on p l a n t tissues has a p p a r e n t l y not yet been studied. T h e results of experiments involving l e a c h i n g of a°nRuc o n t a m i n a t e d soils with a wide v a r i e t y of reagents i n d i c a t e t h a t it is b o u n d e x t r e m e l y tightly. T h e n a t u r e o f the b i n d i n g is n o t p r e s e n t l y well understood.01) I n o r d e r to e l i m i n a t e p e n e t r a tion o f the l e a f cuticle as a possibly i m p o r t a n t factor affecting mobility, e x p e r i m e n t s were done in w h i c h sSSr, 137Cs a n d l°6Ru were i n c o r p o r a t e d into Ceanothus a n d Adenostoma v i a the root systems following w h i c h m o v e m e n t o f the isotopes into new g r o w t h was measured. T h e results of these experiments are presented in T a b l e s 4-6. I t is evident t h a t m u c h g r e a t e r quantities o f
l°6Ru were r e t a i n e d t h a n of either 137Cs or SSSr. T h e a v e r a g e q u a n t i t y p e r p l a n t a m o u n t s in Ceanothus to a b o u t 60 p e r cent a n d in Adenostoma to 67 p e r cent o f the total a m o u n t supplied in the t r e a t m e n t solution (64.8 [xc at harvest). H o w e v e r in b o t h g e n e r a over 90 p e r cent o f the r e t a i n e d dose was found in the root. A l t h o u g h significantly g r e a t e r t r a n s l o c a t i o n to the shoot o c c u r r e d in Ceanothus t h a n in Adenostoma the v e r y low m o b i l i t y o f R u found after foliar a p p l i c a t i o n was confirmed. A p p r o x i m a t e l y 36 p e r cent o f the total 137Cs s u p p l i e d (55.2 ~tc at harvest) was r e t a i n e d b y Ceanothus a n d 15 p e r cent b y Adenostoma. As w i t h l°SRu the 137Cs r e t a i n e d was found p r e p o n d e r a n t l y in the root o f b o t h genera, only a b o u t 20 p e r cent b e i n g in the shoot. T h e c o n c e n t r a t i o n o f laTCs in the new g r o w t h was almost d o u b l e t h a t in the old growth. O n l y 8.6 a n d 5.3 p e r cent of the SSSr s u p p l i e d (28.5 ~tc) were r e t a i n e d b y Ceanothus a n d Adenostoma respectively. H o w e v e r in b o t h g e n e r a a m u c h l a r g e r fraction of the SSSr was found in the shoot t h a n was the case with either l°6Ru or x37Cs. This a m o u n t e d in Ceanothus to 67 p e r cent a n d in Adenostoma to 61 p e r cent o f the r e t a i n e d dose. A l t h o u g h substantial a m o u n t s o f 85Sr were found in the new g r o w t h no preferential c o n c e n t r a t i o n in this fraction was observed. I n
R. HANDLEY and K. L. BABCOCK
582
Table 4. Translocation of SSSr
s6Sr Plant fraction
Dry wt., g
conc., ~Ci/g
s6Sr total in fraction, ~Ci
ssSr, % of retained dose ± S
1.34
(a) Ceanothus I. Old growth 2. Root 3. New growth
15.41 5.18 4.20
0.09 0.16 0.07
0.83 0.28
55.6±4.3 32.6±4"8 11.8±1.1
(b) Adenostoma 1. Old growth 2. Root 3. New growth
14.89 5.18 3.10
0.05 0.11 0.03
0.79 0.61 0.12
54.1±7.6 38.7±5.7 7.2±1.9
laTCs, total in fraction, ~Ci
1~,&, % of
Table 5. Translocation of laTCs Dry wt., g
137Cs conc., ~Ci/g
(a) Ceanothus 1. Old growth 2. Root 3. New growth
28.73 7.99 5.61
0.08 2.07 0.14
2.35 16.45 0.79
12.2±3.0 83.5±5.1 4.2±2.0
(b) Adenostoma 1. Old growth 2. Root 3. New growth
14.44 5.56 2-87
0.09
1.31 6.46 0.52
15.8±0.2 78.2±1.3 6.0±1.2
l°6Ru, total in fraction, ~tCi
l°6Ru, % of
Plant fraction
1.24 0.18
retained dose ± S
Table 6. Translocation of l°6Ru Dry wt., g
lOSRu cone., ~.Ci/g
(a) Ceanothus 1. Old growth 2. Root 3. New growth
20"22 5.84 3"25
0.18 7.20 0'02
3.36 35.87 0.05
8.6 + 1.8 91.3 + 1.9 0.12+0.05
(b) Adenostoma 1. Old growth 2. Root ~. New growth
18.86 5.13 2.84
0.03 8"31 0.01
0.62 43.54 0.04
1.1 +0.5 98.6 _+0.5 0.09 + 0.03
Plant fraction
retained dose ± S
T R A N S L O C A T I O N OF CARRIER-FREE s~Sr, 137Cs AND t°eRu IN WOODY PLANTS ssSr cone., new growth Ceanothus the ratio, sSSr cone., old growth was 0.76 whereas the ratio for a3~Cs was 1.79. T h e ratios calculated for Adenostoma were 0-52 and 1.90 respectively. It will be noted that for these 3 isotopes the relative amounts translocated to the shoot are inversely related to the total amounts retained. This suggests strongly that the relatively great translocation of Sr to the shoot is due to the ease with which it can be displaced by other ions from adsorption sites at the root surface and within the plant. T h e accumulation o f x3~Cs in or on the root and its failure to be transported to the shoot in greater quantities was surprising in view of earlier work(4) showing lzTCs to be metabolically accumulated by barley roots and also in view of the mobility of foliarly applied 137CS in crop plants. (s-9) KLECHKOVSKY and GULIAKIN(~) found that uptake of 1arCs by wheat plants from carrier-free solution was 6 times that of 9°Sr and about 12 times that of X°SRu. O n l y 17 per cent of 137Cs absorbed by wheat was found in the root. W h e t h e r the relatively large quantity of nTCs found associated with the root of Ceanothus and Adenostoma was actually absorbed or was physically b o u n d at the root surface is unknown. T h e results of these experiments a p p e a r to support the supposition that m o v e m e n t offoliarly applied ions at carrier-free levels in Ceanothus and Adenostoma is controlled by the rate of penetration of the leaf and to show that a similar kind of control is exercised at the root. T h e rate of penetration at both sites appears to be in turn related to the binding energies of the ions.
2. BUKOVAC M. J. and WrrrwER S. H. (1957) Absorption and mobility of foliar applied nutrients. Plant Physiol. 329 428-435. 3. HANDL~YR. and OVERSTREETR. (1961) Effect of various cations upon absorption of carrier-free cesium. Plant Physiol. 36, 66M59. 4. HANDLEYR. and OVSP.STREETR. (1968) Uptake of carrier-free 137Cs by Ramalina reticulata. Plant Physiol. 43, 1401-1405. 5. HANDLEY R., SCHULZ R. K., MARSCNNER H., OVERSTREET R. and LONGHURST ~¢. M. (1967)
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REFERENCES
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Translocation of carrier-free snSr applied to the foliage of woody plants. Radiation Botany 7, 91-95. KLECHKOVSiC¢V. M. and GULIAKn~I. V. (1958) Behavior of tracer amounts of strontium, ruthenium, cesium and zirconium in soils and plants according to the data of investigations with radioactive isotopes of these elements, pp. 150-172. In: R. C. EXTE~NN (ed.), Radioisotopes in scientific research, vol. 4. Pergamon Press, Oxford. LEvi E. (1966) Uptake and distribution of xs~Cs applied to leaves of bean plants. Radiation Botany 6, 567-574. MmI)LETON L. J. (1958) Absorption' and trauslocation of strontium and cesium by plants from foliar sprays. Nature 181, 1300-1303. MmDLETON L . J . (1959) Radioactive strontium and caesium in the edible parts of crop plants after foliar contamination. Intern. 07, Radiation Biol. 1,387-402. Mool~v J. and S9.umE H. M. (1963) The entry of strontium into potato tubers after foliar contamination. Radiation Botany 3, 95-98. Scauez R. K. and B~amocK K. L. (1969) Behavior and effects of radionuclides in soils and pIants, pp. I-I0. Project report 1969-70 Contract AT(ll-1)-34, Project No. 23, Atomic Energy Commission. SCrIULZ R. K., OVERSTm~ETR. and B.~O.SHADI. (1960) On the soil chemistry of cesium 137. Soil Science 89, 16-27. SQvm~ H. M. and MmDLETON L. J. (1966) Behaviour of x37Cs in soils and pastures: a long term experiment. Radiation Botany 6, 413--423.
T R A N S L O C A T I O N OF C A R R I E R - F R E E S~Sr, ~ C s AND ~°6Ru IN WOODY PLANTS* R. H A N D L E Y a n 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 8 oTune 1970) A b s t r l c t - - C a r r i e r - f r e e solutions of t87Cs and t°eRu were applied to the foliage of three genera of woody shrubs (Ceanothus, Adenostoma and Quercus) and subsequent translocation into untreated portions of the plants was measured. In all cases the bulk of the retained dose remained with the directly treated material. The results indicate that in these genera foliarly applied x3~Cs is no more mobile than Sr while X°6Ru is considerably less mobile than either. In another series of experiments the distribution of 8~Sr, xn~Cs and X°3Ru between the root, the old growth and the new growth was determined after incorporation of the isotopes into Ceanothus and Adenostoma via their root systems, xsvCs and especially X°eRu were largely retained in the root. A relatively large fraction of the retained dose of SSSr was found in the shoot. In both series of experiments a preferential movement of xS~Cs into new growth was observed. R~mmmg---On a appliqud des solutions de 137Cs et ~°eRu sans entraineur au feuillage de trois genres de plantes ligneuses fourrag6res (Ceanothus, Adenostoma et Quercus). On a ensuite mesur~ leur translocation dans les portions des plantes non traitdes. Dans tousles cas, la majeure partie de la dose retenue reste avec le materiel directement traitS. Les r~ultats indiquent que, dans ces genres, le 13~Cs appliqud au feuillage n'est pas plus mobile que Sr alors que l°eRu est beaucoup moins mobile que l'un ou l'autre isotope. Dans une autre s~rie exp~rimentale, la distribution de ssSr, 137Cs et l°6Ru parmi les vieilles et les nouvelles pousses et les racines &ait d&ermin~e a p r ~ incorporation des isotopes h Ceanothuset Adenostomapar leur syst6me radiculaire. ~sTCs et spdcialement ~°eRu sont fortement retenus par la racine. Une fraction relativement importante de la dose de esSr retenue se retrouve dam le rejeton. Dam les deux s~ries d'exp~rience, on retrouve un mouvement pr~f~rentiel du ~37Cs dans les nouvelles pousses. Z u s a m m e n f a s s u n g - - D a s Blattwerk von drei Arten holziger Futterpflanzen (Ceanothus, Adenostoma und Quercus) wurden mit tr~igerfreien L6sungen yon 137Cs und t°6Ru behandelt und anschliessende Translokation in unbehandelte Teile der Pflanzen wurde gemessen. In allen F~illen blieb der gr6sste Teil der erhaltenen Dosen im direkt behandelten Material. Die Ergebnisse zeigen, dass fiir die Bl/itter dieser Arten angewandte t3~Cs nicht beweglicher ist als Sr, w/ihrend ~°6Ru betr~ichtlich weniger beweglich ist als beide. In einer anderen Reihe yon Experimenten wurde die Verteilung yon S6Sr, xs~Cs und X°6Ru zwischen Wurzel, altem und neuem Wachstum nach der Inkorporation der Isotopen in Ceanothus und Adenostoma durch ihr Wuzelsystem bestimmt. ~37Csund besonders X°nRuwurden weitgehend in der Wurzel zuriickbehalten. Ein verh~iltnism~issig grosser Teil der zuriickbehaltenen Dosis von ~Sr wurde in der Sch6sslingsspitze gefunden. Bei beiden Versuchsreihen wurde eine bevorzugte Bewegung des IS~Csin das neue Wachstum beobachtet. *This report is based on work performed under Contract AT-( 11-1 ) with the United States Atomic Energy Commission. 577
R. HANDLEY and K. L. BABCOCK
578 INTRODUCTION
THE RESULTS of experiments dealing with the translocation of sSSr in 3 genera of xerophytic shrubs eaten by browsing animals were reported previously.(5) In these experiments carrier-free solutions of SSSr were applied to selected portions of the foliage ofCeanothus, Adenostoma and Quercus plants following which movement of the isotope into new growth and other untreated portions of the shoot was measured. The data obtained indicate that Sr is considerably more mobile in Ceanothus and Adenostoma than it has been shown to be in a variety of crop plants. (~,9.,e, s-10) Under field conditions where the plants were subject to occasional wetting, about 6 per cent of the retained dose was found in growth which occurred during the three-month interval between treatment and harvest. The m a x i m u m amounts of s 5Sr translocated from bean and corn leaves (also rewetted periodically during the experiment) were reported by Ambler to be 0.6 and 0"5 per cent of the applied dose respectively.(1) The reason for this difference in behavior is presently unknown. It is the more remarkable since in our experiments with woody shrubs much of the dose was applied to the outer bark rather than being confined to the leaves. Thus it seems likely that an undetermined part of the applied dose was not available for absorption and redistribution. Were it possible to estimate that portion and subtract it from the total dose administered, an even larger translocated percentage would of course be computed. Also, because of the greater development of the leaf cuticle in xerophytic plants such as Ceanothus and Adenostoma absorption and redistribution of ions applied to the leaves would perhaps be expected to be more restricted than in mesophytic crop plants. It is possible however that the failure of mesophytic plants to translocate foliarly applied Sr more readily may not be due primarily to the inability of Sr to penetrate the leaf cuticle, but rather to the active absorption and sequestration of-Sr by the leaf tissue. Levi has presented data suggesting that active accumulation of 134Cs by bean leaves limits translocafion of this isotope.(v) In view of the results obtained in our earlier experiments it became of interest to know to what extent the ability of Ceanothus and Adenostoma to translocate foliarly applied Sr extended to other
fallout components. To investigate this, similar experiments have been done using carrier-free lsTCs and l°6Ru. Translocafion offoliarly applied x37Cs and 134Cs has previously been studied in beans and other crop plants.0,e-o) In these studies Cs has been shown to be more readily absorbed and translocated than Sr. Thus in the experiments conducted by MIDDLETON(8) less than 0.5 per cent of the applied dose of sgSr was found in the tubers of potato plants after foliar contamination whereas 25-30 per cent of the dose was found in the tubers after foliar contamination with 13~Cs. The data presented by KLECHKOVSKY and GULIAKIN(6)indicate that in sunflower and bean l°eRu like °°Sr is not readily translocated from contaminated leaves. The results obtained in the experiments involving foliar applications of ssSr, ls~Cs and ~°6Ru to Ceanothus and Adenostoma suggested that the rate limiting step in absorption and translocation might be the initial penetration of the leaf cuticle. To investigate this the relative mobilities of S~Sr, 137Cs and X°eRu were determined by measuring their movement into new growth after incorporating the isotopes into the plants via the root system rather than the foliage. MATERIALS
AND METHODS
For the experiments involving foliar applications of isotopes the methods were similar to those previously reported.~5) Small specimens of Ceanothus cuneatus, Hook. (Buck Brush), Adenostoma fasciculaturn, H. and A. (Chamise) and Quercus durnosa, Nutt. (Scrub Oak) were transplanted at the Hopland Field Station of the University of California into one-gallon cans and allowed to become well established over a period of several months. In the spring, just prior to the onset of new growth the plants were placed in the greenhouse at Berkeley. Six plants of each species were treated with lSVCs, six with l°6Ru. This was done by painting selected parts of the foliage with carrier-free solutions of laTCsC1 or l°eRuCl3 containing 10~.c per ml. Because the isotopes were received in dilute HCI the diluted solutions used were slightly acid. Neutralization was not deemed desirable because of the effects upon uptake which might have been produced by the introduction of a competing ion. The painted plants became dry within a few minutes
TRANSLOCATION OF CARRIER-FREE ssSr, xaTCs AND X°6Ru IN WOODY PLANTS and no evidence of injury to the treated portions was observed. Removal of HC1 from the solutions by evaporation was not feasible because both ~37Cs and l°eRu are tenaciously held by the walls of containers. After taking carrier-free solutions to dryness large fractions of the activity cannot be redissolved in water. Following treatment and marking of growing points with India ink the cans (perforated at the bottom) were placed in shallow containers (2 in. high) which were kept filled with water. This method of irrigation reduced the danger of wetting the shoots. After 8 weeks the whole aerial portion of each plant of Ceanothus and Adenostoma was separated into 4 fractions: new growth on untreated branches, untreated old growth, new growth on treated branches and treated old growth. The Quercus specimens were very small. For this reason it was practicable in this case to separate only treated old growth and new growth on treated branches. The various fractions were dried at 70°C, ground in an intermediate Wiley mill to pass the 20 M screen and their content of ~87Cs or ~°eRu determined by measuring the g a m m a emission of weighed samples. For study of the translocation of SSSr, x37Cs and l°eRu introduced into the plants via the roots, small specimens of CeanothusandAdenostoma obtained at the Hopland Field Station were transplanted into 4 1. beakers containing I/4 strength Hoagland solution. The roots were washed free of adhering soil before transplanting. The plants were maintained with continuous aeration for two weeks in a lath house. T h e y were protected from rain by means of a shelter made of polyethylene sheeting. This was carried out in February of 1969. The lath house was used rather than a greenhouse because the greater warmth of the latter would have induced the onset of new growth prematurely. After two weeks isotopes were added as carrier-free solutions to the beakers. Three plants of each genus were treated with each isotope. The initial concentrations of isotopes in the nutrient media were as follows: ssSr, 13.9 ~tc/1; l°eRu, 18"7 ~tc/1 and laTCs, 14.3 ~tc/1. The p H was about 5.5. The plants were allowed to remain in the radioactive solutions for one month, at the end of which the beginning of new shoot growth was apparent. The roots were then washed with five 41. changes
579
of 0.01 N CaCI 2 and the plants were transplanted into non-radioactive 1/2 strength Hoagland solutions. At this time the growing points of each plant were marked with India ink and all plants were removed to the greenhouse in order to promote more rapid growth. After 5 weeks each plant was cut into 3 fractions representing old shoot growth, new shoot growth and total root. The fractions were dried, ground and analyzed as described above. Some confusion m a y be occasioned by the use of the term "dose". In this paper (as in m a n y others) this word designates a quantity of a radionuclide measured in microcuries. The same word is of course also in general usage to mean radiant energy absorbed per g.
RESULTS AND DISCUSSION
The results of experiments with foliarly applied 13~Cs are presented in Tables 1 and 2. It is apparent that as in the earlier experiments with 85Sr¢5) the bulk of the laTCs applied remained with the directly treated material, over 98 per cent of the retained dose being found in this fraction of all 3 genera. In Ceanothus 1-6 per cent of the laTCs retained was found distributed among the untreated fractions after 8 weeks. The corresponding figure for ssSr(S) was 3"2 per cent. In Ceanothus the mobility of 85Sr thus apparently exceeds that ofl37Cs. In Adenostoma the mobilities measured in this way were about equal while in Quercus the mobility of 137Cs was slightly greater than that of SSSr. These results are strikingly different to those obtained by MIDDLEToN(S, 9) and othersll,2,6,1°) which indicate that in potatoes and other crop plants foliarly applied carrier-free Sr is virtually immobile while 137Cs is readily translocated from the site of contamination. Although in Ceanothus and Adenostoma the amounts of 137Cs and ssSr translocated (expressed as per cent of the retained dose) are similar the distributions of the two isotopes within the untreated material are quite different. This is apparent in the data of Table 2. The tendency of 137Cs to accumulate in younger or actively growing tissue is well expressed in both Ceanothus and Adenostoma. 85Sr tended to move acropetally into contiguous new growth and basipetally into untreated old growth in about
R. HANDLEY and K. L. BABCOCK
580
Table 1. Translocation of 127Cs applied to thefoliage of woodyforage plants Dry wt., g
laTCs cone., ~tCi/g
x37Cs total in fraction, btCi
12'Cs, % of retained dose ± S
(a) Ceanothus I. Old growth, treated 2. Old growth, untreated 3. New growth, treated branches 4. New growth, untreated branches
6.24 5.62 0.78 0.57
4"21 -+ 102 0'97 37"64 2'00
21"97 × 102 5"18 25.59 1"04
98.41 _+ 1.13 0.32 _+0.28 1.29 + 0.82 0.04-+ 0.03
(b) Adenostoma 1. Old growth, treated 2. Old growth, untreated 3. New growth, treated branches 4. New growth, untreated branches
2.91 1-72 0.94 0.69
4"78 x lOs 1.52 10"91 1.58
10"91 × lOs 2'92 11"88 0"96
99.00 _+0.92 0.20_+0.18 0.88 _+0.65 0.06 _+0.04
(c) Quercus 1. Old growth, treated 2. New growth, treated branches
0.49 0.35
9.15 x 102 16.29
3.94× 102 4.33
98.34_+2.18 1.24_+ 1.02
Plant fraction
Table 2. Distribution of translocated ssSr, 13~Csand *°SRu after foliar contamination % of translocated dose x87Cs lO6Ru
Plant fraction
ssSr
(a) Ceanothus 1. Old growth, untreated 2. New growth, treated branches 3. New growth, untreated branches
50.0 46.8 3.2
16.3 80.6 3.3
61.6 31.9 8.0
(b) Adenostoma 1. Old growth, untreated 2. New growth, treated branches 3. New growth, untreated branches
58.0 34.5 7.6
18.5 75.4 6.1
47.4 39.1 13.5
equal amounts.(5) M o v e m e n t o f 137Cs was pred o m i n a n t l y into the new growth, 80.6 a n d 75.4 p e r cent o f the translocated 13~Cs being found in this fraction of Ceanothus a n d Adenostoma respectively. Note also ( T a b l e 1) t h a t the conc e n t r a t i o n oflSTCs in the new g r o w t h o f u n t r e a t e d branches exceeds t h a t in the old growth. T h e d a t a suggest t h a t while foliarly a b s o r b e d Sr is distributed b y diffusion a n d convectively in the t r a n s p i r a t i o n stream, the distribution o f Cs m a y involve in p a r t a m e t a b o l i c a l l y m e d i a t e d transp o r t process w h i c h concentrates this ion in actively g r o w i n g tissue. T h e translocation o f
foliarly a p p l i e d 137Cs b y p o t a t o plants to d e v e l o p i n g tubers r a t h e r t h a n solely to transp i r i n g parts of the plants has been n o t e d b y MIDDLETON. (s, 9) O n l y a v e r y slight t r a n s l o c a t i o n o f X°SRu o c c u r r e d in all three g e n e r a with no evidence of preferential m o v e m e n t into new g r o w t h ( T a b l e 3). This is in accord w i t h the low m o b i l i t y of l°SRu a p p l i e d to the leaves of b e a n a n d sunflower r e p o r t e d b y KLECHKOVSKY a n d G U L I A K I N . (e)
T h e d a t a o b t a i n e d i n d i c a t e the following o r d e r o f m o b i l i t y with respect to foliar a p p l i c a t i o n :
T R A N S L O C A T I O N OF C A R R I E R - F R E E ssSr, 187Cs AND X°6Ru IN W O O D Y PLANTS
581
Table 3. Transloeation of l°6Ru applied to thefoliage of woodyforage plants Dry wt., g
X°SRu cone., ~tCi/g
X°6Ru, total in fraction, ~tCi
i°6Ru, % of retained dose _+S
(a) Ceanothus 1. Old growth, treated 2. Old growth, untreated 3. New growth, treated branches 4. New growth, untreated branches
5.48 4.52 0.51 0.88
5.96 x 102 0.53 2-73 0.49
25.47 x 10 ~ 2.47 1.31 0.33
99.90 + 0.16 0. i 1 + 0.068 0"09 + 0-13 0.01 + 0.007
(b) Adenostoma 1. Old growth, treated 2. Old growth, untreated 3. New growth, treated branches 4. New growth, untreated branches
3.68 2.09 1.30 0.90
5.40 × 10 ~ 0.65 0.65 0.35
19.26 x 102 1.20 0.99 0.34
99.86 + 0-06 0-07 + 0.05 0.08 + 0.08 0.05 + 0.14
(c) Quercus 1. Old growth, treated 2. New growth, treated branches
0.61 0.52
10.04 × 102 0.09
4.83 × I02 0.06
NI00 < 0.01
Plant fraction
S r . ~ C s > ~ R u . I n view of the relatively high m o b i l i t y o f f o l i a r l y a p p l i e d Cs r e p o r t e d for mesop h y t i c plants, the results o b t a i n e d here suggest t h a t in Ceanothus a n d Adenostoma the a p p a r e n t mobilities o f these ions m a y reflect largely the rates at w h i c h they p e n e t r a t e the l e a f cuticle a n d in t u r n their b i n d i n g energies at the leaf surface. Cs is k n o w n to be a d s o r b e d m u c h m o r e strongly than Sr b o t h to soil colloids(X2,13) a n d to p l a n t tissue33, 4) T h e failure of foliarly a p p l i e d xzTCs to be t r a n s l o c a t e d as r e a d i l y as it is in crop plants m a y reflect differences in the composition or structure of the l e a f cuticle in xerophytes as comp a r e d to mesophytic plants. T h e b e h a v i o r of X°eRu with respect to a d s o r p t i o n on p l a n t tissues has a p p a r e n t l y not yet been studied. T h e results of experiments involving l e a c h i n g of a°nRuc o n t a m i n a t e d soils with a wide v a r i e t y of reagents i n d i c a t e t h a t it is b o u n d e x t r e m e l y tightly. T h e n a t u r e o f the b i n d i n g is n o t p r e s e n t l y well understood.01) I n o r d e r to e l i m i n a t e p e n e t r a tion o f the l e a f cuticle as a possibly i m p o r t a n t factor affecting mobility, e x p e r i m e n t s were done in w h i c h sSSr, 137Cs a n d l°6Ru were i n c o r p o r a t e d into Ceanothus a n d Adenostoma v i a the root systems following w h i c h m o v e m e n t o f the isotopes into new g r o w t h was measured. T h e results of these experiments are presented in T a b l e s 4-6. I t is evident t h a t m u c h g r e a t e r quantities o f
l°6Ru were r e t a i n e d t h a n of either 137Cs or SSSr. T h e a v e r a g e q u a n t i t y p e r p l a n t a m o u n t s in Ceanothus to a b o u t 60 p e r cent a n d in Adenostoma to 67 p e r cent o f the total a m o u n t supplied in the t r e a t m e n t solution (64.8 [xc at harvest). H o w e v e r in b o t h g e n e r a over 90 p e r cent o f the r e t a i n e d dose was found in the root. A l t h o u g h significantly g r e a t e r t r a n s l o c a t i o n to the shoot o c c u r r e d in Ceanothus t h a n in Adenostoma the v e r y low m o b i l i t y o f R u found after foliar a p p l i c a t i o n was confirmed. A p p r o x i m a t e l y 36 p e r cent o f the total 137Cs s u p p l i e d (55.2 ~tc at harvest) was r e t a i n e d b y Ceanothus a n d 15 p e r cent b y Adenostoma. As w i t h l°SRu the 137Cs r e t a i n e d was found p r e p o n d e r a n t l y in the root o f b o t h genera, only a b o u t 20 p e r cent b e i n g in the shoot. T h e c o n c e n t r a t i o n o f laTCs in the new g r o w t h was almost d o u b l e t h a t in the old growth. O n l y 8.6 a n d 5.3 p e r cent of the SSSr s u p p l i e d (28.5 ~tc) were r e t a i n e d b y Ceanothus a n d Adenostoma respectively. H o w e v e r in b o t h g e n e r a a m u c h l a r g e r fraction of the SSSr was found in the shoot t h a n was the case with either l°6Ru or x37Cs. This a m o u n t e d in Ceanothus to 67 p e r cent a n d in Adenostoma to 61 p e r cent o f the r e t a i n e d dose. A l t h o u g h substantial a m o u n t s o f 85Sr were found in the new g r o w t h no preferential c o n c e n t r a t i o n in this fraction was observed. I n
R. HANDLEY and K. L. BABCOCK
582
Table 4. Translocation of SSSr
s6Sr Plant fraction
Dry wt., g
conc., ~Ci/g
s6Sr total in fraction, ~Ci
ssSr, % of retained dose ± S
1.34
(a) Ceanothus I. Old growth 2. Root 3. New growth
15.41 5.18 4.20
0.09 0.16 0.07
0.83 0.28
55.6±4.3 32.6±4"8 11.8±1.1
(b) Adenostoma 1. Old growth 2. Root 3. New growth
14.89 5.18 3.10
0.05 0.11 0.03
0.79 0.61 0.12
54.1±7.6 38.7±5.7 7.2±1.9
laTCs, total in fraction, ~Ci
1~,&, % of
Table 5. Translocation of laTCs Dry wt., g
137Cs conc., ~Ci/g
(a) Ceanothus 1. Old growth 2. Root 3. New growth
28.73 7.99 5.61
0.08 2.07 0.14
2.35 16.45 0.79
12.2±3.0 83.5±5.1 4.2±2.0
(b) Adenostoma 1. Old growth 2. Root 3. New growth
14.44 5.56 2-87
0.09
1.31 6.46 0.52
15.8±0.2 78.2±1.3 6.0±1.2
l°6Ru, total in fraction, ~tCi
l°6Ru, % of
Plant fraction
1.24 0.18
retained dose ± S
Table 6. Translocation of l°6Ru Dry wt., g
lOSRu cone., ~.Ci/g
(a) Ceanothus 1. Old growth 2. Root 3. New growth
20"22 5.84 3"25
0.18 7.20 0'02
3.36 35.87 0.05
8.6 + 1.8 91.3 + 1.9 0.12+0.05
(b) Adenostoma 1. Old growth 2. Root ~. New growth
18.86 5.13 2.84
0.03 8"31 0.01
0.62 43.54 0.04
1.1 +0.5 98.6 _+0.5 0.09 + 0.03
Plant fraction
retained dose ± S
T R A N S L O C A T I O N OF CARRIER-FREE s~Sr, 137Cs AND t°eRu IN WOODY PLANTS ssSr cone., new growth Ceanothus the ratio, sSSr cone., old growth was 0.76 whereas the ratio for a3~Cs was 1.79. T h e ratios calculated for Adenostoma were 0-52 and 1.90 respectively. It will be noted that for these 3 isotopes the relative amounts translocated to the shoot are inversely related to the total amounts retained. This suggests strongly that the relatively great translocation of Sr to the shoot is due to the ease with which it can be displaced by other ions from adsorption sites at the root surface and within the plant. T h e accumulation o f x3~Cs in or on the root and its failure to be transported to the shoot in greater quantities was surprising in view of earlier work(4) showing lzTCs to be metabolically accumulated by barley roots and also in view of the mobility of foliarly applied 137CS in crop plants. (s-9) KLECHKOVSKY and GULIAKIN(~) found that uptake of 1arCs by wheat plants from carrier-free solution was 6 times that of 9°Sr and about 12 times that of X°SRu. O n l y 17 per cent of 137Cs absorbed by wheat was found in the root. W h e t h e r the relatively large quantity of nTCs found associated with the root of Ceanothus and Adenostoma was actually absorbed or was physically b o u n d at the root surface is unknown. T h e results of these experiments a p p e a r to support the supposition that m o v e m e n t offoliarly applied ions at carrier-free levels in Ceanothus and Adenostoma is controlled by the rate of penetration of the leaf and to show that a similar kind of control is exercised at the root. T h e rate of penetration at both sites appears to be in turn related to the binding energies of the ions.
2. BUKOVAC M. J. and WrrrwER S. H. (1957) Absorption and mobility of foliar applied nutrients. Plant Physiol. 329 428-435. 3. HANDL~YR. and OVERSTREETR. (1961) Effect of various cations upon absorption of carrier-free cesium. Plant Physiol. 36, 66M59. 4. HANDLEYR. and OVSP.STREETR. (1968) Uptake of carrier-free 137Cs by Ramalina reticulata. Plant Physiol. 43, 1401-1405. 5. HANDLEY R., SCHULZ R. K., MARSCNNER H., OVERSTREET R. and LONGHURST ~¢. M. (1967)
6.
7.
8.
9.
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12.
REFERENCES
1. AMBLER J. E. (1964) Translocation of strontium from leaves of bean and corn plants. Radiation Botany 4, 259-265.
583
13.
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