THE EFFECT OF GIBBERELLIC ACID, KINETIN AND INDOLYLACETIC ACID ON THE LATERAL MOVE- MENT OF LABELLED PLANT GROWTH REGULA- TORS IN WILLOW STEMS
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1 New Phytol. (1973) 72, THE EFFECT OF GIBBERELLIC ACID, KINETIN AND INDOLYLACETIC ACID ON THE LATERAL MOVE- MENT OF LABELLED PLANT GROWTH REGULA- TORS IN WILLOW STEMS BY R. J. FIELD Department of Plant Science, Liticoln College, Canterbury, New Zealand {Received 17 November 1972) SUMMARY Using willow stem segments it has been possible to show that the presence of gibberellic acid in the xylem can influence the lateral mobility of radioactive indolylacetic acid and its principal metabolite, indoleacetylaspartic acid. The extent of the lateral movement of indolylacetic acid depends on the concentration of endogenous gibberellin in the xylem, and movement may be increased by exogenous gibberellin applications to the xylem. The mechanism controlling the lateral movement of 2,4-dichlorophenoxyacetic acid and 2,4,5-trichlorophenoxyacetie acid appeared to be somewhat different and there was no positive movement towards gibberellin. These results are discussed in relation to previous experimentation on the interaction of plant growth regulators during transport. It is suggested that gibberellins may influence cell membranes and this may account for their effects on the transport of indolylacetic acid. INTRODUCTION Several workers have shown that growth regulators may interact in transport phenomena wben applied simultaneously to plant tissues. Thus the movement of IAA may be modified by the cytokinin, kinetin (McCready, Osborne and Black, 1965; Davies, Seth and Wareing, 1966) and by gibberellin (Jacobs and Case, 1965). Similarly Niedergang- Kamien and Leopold (1959) showed that two auxin-type substances, IAA and 2,4-D may interact in transport phenomena. There have been a number of investigations of hormone-directed transport of sugars and ions in which the hormone and mobile substance are spatially separated by plant tissue at the start of the experiment (Seth and Wareing, 1967; Lepp and Peel, 1970; Bowen and Wareing, 1971). This experimental approach has not been used to study the effect of one growth hormone on the movement of another. The present experiments were designed to determine whether the phenomenon of hormone-directed transport of growth hormones exists. Previous experiments using willow stem material (Field and Peel, 1971a, b, 1972) have shown that exogenously applied IAA, 2,4-D and 2,4,5-T will move both laterally in parenchyma and longitudinally in sieve tubes. However, no attempt was made to examine factors, hormonal or otherwise, that may be controlling the movement of the growth regulators. It is obvious from the wealth of published material available that the movement of growth hormones from their site of synthesis to site of action is vital in controlling innumerable physiological responses in plants. In a recent publication, Shein and Jackson 471
2 472 R. J. FIELD (1971) postulated that apical dominance in plants may be controlled by a specific balance of hormones at certain physiologically active sites. For such a hypothesis to operate the hormone levels could be controlled by carefully balancing their synthesis and removal by detoxification mechanisms. However, hormone levels could be further regulated by transporting excess hormones away to physiologically inactive situations, and it is further postulated that this process may be controlled by other chemically unrelated growth hormones. Phillips (1969) has already suggested that movement of endogenous cytokinins may be controlled by apically synthesized auxin and that this may be a component in the regulation of apical dominance. Similarly, Jackson (1968) suggested that gibberellins may increase auxin movement to tissues surrounding tbe seed in stonefruit. One valid criticism of experiments designed to examine hormone-directed transport of sugars and ions is that the hormones may initiate a 'growth sink' towards which the ions and sugars move. By using mature willow stem segments in the present experiments rather than herbaceous material, it is hoped that this complication has been avoided. MATERIALS AND METHODS Mature stems (2-4 year old") of Salix fragilis L. were rooted and grown in water culture after collection from tbe field. The willow stems were then cut into segments, generally between 8 and 12 cm in length and 1.5 cm in diameter. The xylem of isolated stem segments was perfused with unlabelled, aqueous solutions of indolylacetic acid (IAA), kinetin, gibberellic acid (GA) or distilled water until 15 ml of xylem effluent bad been collected. The stem segments were supplied either with water or the appropriate solution of growth regulator from rubber tubing fitted over tbe morpbological apex and base. In the experiments in which the lateral movement of growth regulators from the bark to the xylem stream was measured, the xylem was perfused in the manner described by Field and Peel (1971a). Tbe GA and distilled water were supplied to individual stem segments from separate reservoirs and xylem effluent samples were collected in beakers mounted on a turntable coupled to a timer unit, thus enabling collections to be made over known intervals of time. Unlabelled solutions of IAA and GA were made by dissolving tbe solid material in a small volume of absolute methanol, the solution was diluted with distilled water to give a final methanol concentration of 0.5%. Kinetin was dissolved in a small volume of i N hydrochloric acid before dilution with distilled water, to give a final hydrochloric acid concentration of 0.2%,. The following labelled growth regulators were used at the stated specific activities: IAA[i-"*C] (59 mci/mm), 2,4-D[i "'C] (34 mci/mm), 2,4,5-T[i-'*C] (30 mci/nim). Solutions of the three compounds were prepared as described previously (Field and Peel, 1971a) and were used at a radioactive concentration of 5.0 /jci/ml. Application of the labelled compounds to the bark was effected by removing a i cm^ region of outer cortical tissue, ringing the abraded area with anhydrous lanolin and applying 10/d (200/d in continuous perfusion experiments) of the labelled solution to the abraded bark within the lanolin ring. A glass coverslip was placed on the lanolin ring to prevent evaporation. All labelled compounds were extracted from bark and wood tissues in 70% etbanol for 7 days at 5" C. From each stem segment the entire bark (including the point of application of the labelled regulator) and wood were extracted separately. All samples of xylem effluent and tissue extracts were concentrated by evaporation under reduced pressure. Xylem effluent and tissue extract samples were examined by descending cbromatography
3 Lateral movement of growth regulators 473 on Whatman No. i paper using isopropanol:ammonia:water (10:1:1) as the solvent system. The concentration of GA in xylem effluent samples was estimated with the barley endosperm bioassay(coombe, Cohen and Paleg, 1967a, b). Each 15-ml effluent sample was adjusted to ph 2.5 and partitioned twice with 6 ml of ethyl acetate, to remove sugar material. Subsequent analysis showed the complete absence of sugars in the ethyl acetate fractions. After evaporating the ethyl acetate fractions to dryness the solid material was redissolved in distilled water and bioassayed. No attempt was made to precisely characterize the gibberellins in the xylem effluent. RESULTS The lateral movement of IAA, 2,4-jD and 2,4,5-T' in isolated segments In the initial experiments io-cm-iong stem segments were perfused with a solution containing distilled water or combinations of IAA, kinetin and GA, each at i.o x 10"''* M. Lateral movement of ['*C] IAA, 2,4-D or 2,4,5-T was allowed to take place for a period of 24 hours, before bark and wood were separated, extracted, and the activities of the extracts determined. The data are presented in Tables i and 2, the mobility of each compound being measured by the ratio, total activity in wood/total activity in bark. The Table i. The relative mobility of activity derived from IAA between the bark and ivood Perfusion treatment Control (unperfused) GA GA and kinetin Distilled water Kinetin Relative mobility of IAA and metabolite IAAasp (total activity in wood/total activity in bark) O-337 a a b c c Percentage of total activity in the form of IAAasp Bark Wood S Each value is the mean from eight segments. Treatments with no common letter are significantly different at the 5% level. lateral movement of IAA was increased by perfusion with GA and to a lesser extent by a combination of GA and kinetin, whilst perfusion with kinetin alone had little effect. As has previously been determined for Salixviminalis L. (Field and Peel, i97ia)indoleacetylaspartic acid (IAAasp) was the only significant metabolite of IAA detected. The data in Table i also indicated that the percentage of applied IAA metabolized to IAAasp remained constant, irrespective of the perfusion treatment. Thus it would seem that the movement of IAAasp was qualitatively similar to IAA in respect of the perfusion treatments. Unlike the situation for IAA there was no significant metabolism of 2,4-D and 2,4,5-T. The lateral movement of 2,4-D and 2,4,5-T was unaffected by perfusion with GA, whilst perfusion with either IAA or kinetin tended to reduce lateral movement in both eases. The results of experiments using ['*C]IAA may indicate that perfusion with distilled water has removed a factor which affected the lateral movement of IAA. However, the status quo could be reinstated by perfusing the xylem with GA. In order to investigate further the action of GA on IAA movement the above experiment was repeated using a
4 474 R-J- FIELD series of GA concentrations (i x io~^ to i x lo"'^ M). Tbe data from these experiments are presented in Table 3, the mobility of IAA again being measured by the ratio, total activity in wood/total activity in bark. The results show that increases in the lateral movement of IAA are correlated with increases in GA concentration of the perfusion solution. Gibberellin concentrations of i.oxio"-' M and i.oxio"'* M induced a significantly greater lateral movement of IAA than when the xylem was perfused with distilled water. A GA concentration of i.o x io"*" proved to be ineffective in directing IAA movement. As in the initial experiments the degree of metabolism of IAA to IAAasp was similar for all treatments. Table 2. The relative mobilities of 2,4-D and 2,4,5-T between the bark and wood Perfusion treatment Distilled water GA IAA Kinetin Control (unperfused) Relative mobility (total activity in wood/total activity in bark) 2,4-D a a b b b 2,4,5-T a a b b a Eacb value is the mean from eight segments. Treatments witb no common letter are significantly different at the 1% level for 2,4-D and 5% level for 2,4,5-T. Differences between means for the 2,4-D and 2,4,5-T experiments were not compared. Table 3. The relative mobility of activity derived from IAA between the bark and wood, after perfusing the xylem with varying concentrations of GA Perfusion treatment 10-^ M GA io-*m GA IO"* M GA Control (unperfused) Distilled water 10-'' M GA Relative mobility of IAA and metabolite IAAasp (total activity in wood/total activity in bark) a ' ab ab b O.I 13 b Percentagi; of total activity in tbe form of ] IAAasp Bark Wood Each value is the mean from six segments. Treatments with no common letter are significantly different at the 5% level. The lateral movement of IAA into the xylem stream In previous studies on the movement of growth regulators in willow. Field and Pec! (1971a) used a continuous perfusion technique arranged to resemble the movement of xylem water in a transpiring plant. This experiment was designed to see if the gibbcrellin-directed transport of IAA occurred when solution was moving tbrough the xylem. The results given in Fig. 1 show that both IAA and IAAasp moved into the xylem stream more readily when the latter was perfused with i.0 x 1 o " * M GA than with distilled water. Again the percentage of applied IAA metabolized to IAAasp in the bark (approximately 79%) and in the wood (approximately 62%) is similar, irrespective ofthe perfusion treatment.
5 Lateral movement of growth regidators Time (hours) Fig. I. The lateral movement of [i~'''c]iaa (solid symbols) and its metabolite la.<\asp (open symbols), after perfusion of the xylem with either distilled water (circles) or a l x io"-* M solution of GA (triangles). Xylem effluent samples were taken at 6 hourly intervals for 30 hours. 0.4r -o I IxlO-" 1x10-' IxlO" I XiO 1x10' Gibberellin (g/iomi xylem effluent) Fig. 2. Relationship between the lateral movement of [i '*'C]IAA (and IAAasp as metabolite) from the bark to the wood (presented as a ratio of specific activities, wood/bark), and the endogenous gibberellin levels in the xylem. The F-test of goodness of fit is significant at the iv level.
6 476 R. J. FIELD The lateral movement of IAA in response to varying levels of endogenous GA in the xylem Thus far the results have implied that an artificially increased level of GA in the xylem sap may increase the lateral movement of IAA and its metabolite IAAasp. However, this situation may not necessarily be the case in the intact plant. Undoubtedly perfusion ofthe xylem with distilled water or a GA solution removes substances that may also have a measure of control on the lateral movement of IAA, and thus to overcome any differences between tbe natural and experimental situations the following experiments were carried out. Paired stem segments were cut from a single stem and one segment of each pair was perfused with distilled water and the GA content of the effluent was determined using the barley endosperm bioassay. The lateral movement of [' ""^CJIAA was measured in tbe unperfused segment for a period of 24 bours, it being assumed that the GA level in this segment was the same as that in the perfused segment. As may have been predicted from the results of previous experiments, the endogenous GA levels in the xylem sap were related to IAA mobility. To increase the possibility of obtaining a wider range of endogenous GA levels the paired stem segments were taken from a greater variety of willow material. The willow material used in the subsequent experiments had been aged in water culture for varying periods of time or was collected from tbe field immediately prior to use. The results presented in Fig. 2 show a significant linear relationship between endogenous gibberellin levels in the xylem and the movement of '*C label from the bark to the wood. No attempt was made to determine the composition of the ''*G label in all segments, but in tbose tbat were investigated approximately 45% of the label was IAA, the remainder being IAAasp. DISCUSSION (jibbercllic acid appears to influence tbe lateral movement of IAA and its principal metabolite IAAasp in willow stems. Field and Peel (1971a, b, i<)'j2) presented evidence for the mobility of IAAasp and the present results substantiate these original findings. Qualitatively the pattern of movement of IAAasp was similar to that found for IAA in all respects, both compounds were directed towards GA. When the xylem was perfused with kinetin and GA rather than GA alone there was a significant reduction in the lateral movement of IAA and IAAasp. The significance of this result is not clear but further experimentation is in progress. However, the movement of the two chlorophenoxy herbicides 2,4-1) and 2,4,5-T in response to similar GA treatments showed a different result to that found for IAA (I'ables 1 and 2). The significance of these differences is obscure, but suggests that the movement of the two auxin analogues is influenced by a different mechanism to that employed by IAA. Perfusion of the xylem with distilled water presumably removes a higb proportion of endogenous growth promoters, such as GA, and growth inhibitors such as abscisic acid (Bowen and Hoad, 1968). The differences in mobility of IAA and the two chlorophenoxy compounds after xylem perfusion witb distilled water may be indicative of a fundamental difference in their response to the endogenous growth promoters and growth inhibitors in the xylem. One possible mode of action of gibberellin in tbe plant is that it exerts its physiological effects by altering the auxin status ofthe plant tissues. There are a number of instances in which gibberellin increases endogenous auxin level (Kuraishi and Muir, 1963; Nitsch and Nitsch, 1959). It has been assumed that the gibberellin-induced increase in auxin level is due to accelerated auxin synthesis or reduced detoxification. The present results suggest that these increases in IAA may also be due to gibberellin-directed transport of
7 Lateral movement of growth regulators 477 auxin. Whilst this suggestion may explain the increase in auxin in the gibberellin-treated region, it does not offer an explanation of how the induced transport is accomplished. Previous experiments designed to investigate the effect of GA and other growth regulators on the movement of IAA have involved simultaneous application of all compounds to one site (Jacobs and Case, 1965; Pilet, 1965). Tbe present experiments were designed to spacially separate all growtb regulators at the start of the experiment. However, it is not discounted that the GA may have moved laterally to the site of IAA application and by so doing the situation may have been similar to that used by previous workers. Owing to the non-availability of labelled GA the relevance of GA movement to the observed results is unknown. However, these deliberations bring us no closer to an explanation of the present results. Unfortunately there is a dearth of experimental information on the effects of plant growth regulators on cell membrane permeability, although the present results may well be explained by such a phenomena. Luttge, Bauer and Kohler (1968) have suggested that GA may affect cell membrane permeability and generally act upon transport mechanisms. Their conclusions are based on results that showed that K^ ions moved more rapidly in GA treated pea plants than in control plants. Earlier Pilet (1965) had shown that uptake and basipetal transport of IAA in stem sections of Lens culinaris was greater when they had previously been incubated in a GA solution for 2 hours. The effect of GA on cell membrane permeability may well explain both Pilet's and the present results. Obviously an intensive investigation of the relationships between growth regulators and cell membranes and its bearing on transport pbenomena is required. ACKNOWLEDGMENTS I would like to thank Mr K. Rooney for technical assistance. REFERENCES BowEN, M. R. & HoAD, G. V. (1968). Inhihitor content of phloem and xylem sap ohtained from willow {Salix viminalis L.) entering dormancy. Planta, 81, 64. BowEN, M. R. & WAREING, P. F. (1971). Further investigations into hormone-directed transport in stems. Planta, 99, 120. CooMBE, B. G., COHEN, D. & PALEG, L. G. (1967a). Barley endosperm hioassay for gihherellins. L Parameters of the response system. PL PhysioL. Lancaster, 42, 105. CooMBE, B. G., COHEN, D. & PALEG, L. G. (i967h). Barley endosperm hioassay for gihherellins. 11, Applieation of the method. PL PhysioL, Lancaster, 42, 113. DAVIES, C. R., SETH, A. K. & WAREING, P. F. (1966). Auxin and kinetin interaction in apical dominance Science, N.Y., 151, 468. FIELD, R. ]. & PEEL, A. J. (1971a). The metaholism and radial movement of growth regulators and herbicides in willow stems. New PhytoL, 70, 743. FIELD, R. J. & PEEL, A. ]. (i97ih). The movement of growth regulators and herbicides into the sieve elements of willow. New PhytoL, 70, 997. FIELD, R. J. & PEEL, A. J. (1972). The longitudinal mobility of growth regulators and herbicides in sieve tubes of willow. New PhytoL, 71, 249. JACKSON, D. I. (1968). Gibberellin and growth in stonefruits: induction of parthenocarpy in plum. Aust.J. biol. Sci., 21, JACOBS, W. P. & CASE, D. B. (1965). Auxin transport, gibberellin, and apical dominance. Science, N. Y., 148, KuRAISHI, S. and Mum, R. M. (1963). Diffusible auxin increase in a rosette plant treated with gihberellin. Ndturwissenschaften. 50, 337. LEPP, N. W. & PEEL, A. J. (1970). Some effects of IAA and kinetin upon the movement of sugars in the phloem of willow. Planta, 90, 230. LUTTGE, U., BAUER, K. & KOHLER, D. (1968). Fruhwirkungen von gihberellinsaure auf membrantransporte in jungen Erbsenpflanzen. Biochim. Biophys. Acta., 150, 452. MCCREADY, C. C, OSBORNE, D. J. & BLACK, M. K. (1965), Promotion by kinetin of the polar transport of two auxins. Nature, Lond., 208, 1065.
8 478 R. J. FIELD NIKDERGANG-KAMIEN, E. & LEOPOLD, A. C. (1959). The inhibition of transport of indoleacetic acid by pbenoxyacetic acids. Physiologia PL, 12, 776. NITSCH, J. P. and NITSCH, C. (1959). Modification du metabolisme des auxines par l'acide gibberellique. Bull. Soc. fr. PhysioL veg., 5, 20. PHILLIPS, 1. D. J. (1969). Apical dominance. In: The Physiology of Plant Grozvth and Development (Ed. by M. B. Wilkins), pp McGraw-Hill, London. PiLET, P. E. (1965). Polar transport of radioactivity from '*C-labe!led-^-indolylacetic acid in stems of Lens cidinaris. Physiologia PL, 18, 687. SliTH, A. K. & WAKEING, P. F. (1967). Hormone-directed transport of metabolites and its possible role in plant senescence, jf. exp. Bot., 18, 65. SHEIN, T. & JACKSON, 13. I. (1971). Hormone interaction in apical dominance in Phaseohis vulgaris L. Ann. Bot., N.S. 35, 555.
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