EVIDENCE ON THE SITE OF ACTION OF GROWTH RETARDANTS 1

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1 Plant & Cell PhysioL, 6 (1965) EVIDENCE ON THE SITE OF ACTION OF GROWTH RETARDANTS 1 ROBERT CLELAND 2 Department of Botany, University of California, Berkeley, Calif., U.S.A. (Received May 18, 1964) 1. The ability of five growth retardants to inhibit the GA-induced and endogenous growth of Avena leaf sections has been investigated. The retardants vary in effectiveness. The order, from most effective to least, is Phosfon D, Amo-1618, C11, CCC and B The inhibition of growth caused by Phosfon D and Amo-1618 is not reversed by GA. It is apparent that the retardants do not compete with GA at the site of GA-action. 3. Addition of IAA will partially reverse the inhibition induced by Phosfon D or Amo It is concluded that the retardants act in part in Avena leaf sections by interfering with the auxin metabolism of the tisssue. In recent years, a variety of compounds have been shown to possess growth retardant ability (2). Among these compounds are Amo-1618 (2), CCC (3), Phosfon D (4), B995, and COU (5). Because the effects of these compounds on growth (1, 2, 6, 7), flowering (5) and enzyme levels (9) can be counteracted by gibberellins, they have been called antigibberellins (7, 9). The site of action of the growth retardants is not known. It might be located anywhere along the chain of reactions leading from GA to growth. A variety of steps have been proposed as the site of action. For example, it has been suggested that these compounds inhibit GA synthesis (1), competitively antagonize GA at the site of its action or affect some facet of the auxin metabolism of the tissue (9,11). With the systems that have been examined to date it has not been possible to separate these possibilities. In this study a test was made of the ability of growth retardants to compete with GA at its site of action. The GA-induced Avena leaf elon- Abbreviations: Amo-1618, 2-isopropyl-4-dimethylamino- 5- methylpheny 1-1-piperidinecarboxylate methyl chloride; CCC, (2-chloroethyl) trimethyl-ammonium chloride; Phosfon D (PD), 2,4-dichlorobenzyl-tributylphosphonium chloride; B995, N-dimethylamino succinamic acid; C11, N-dimethylamino maleamic acid; IAA, indoleacetic acid; GA, gibberellic acid.» Supported in part by grants G and GB-195 from the National Science Foundation. 2 Present address: Department of Botany, University of Washington, Seattle, Washington.

2 8 R. CLELAND Vol. 6 (1965) gation system has been used since it is possible with this system to distinguish between the various possibilities (12). Effects on GA synthesis can be eliminated since the growth occurs in response to exogenous rather than endogenous GA. The action of GA and auxin on this system can easily be differentiated. This makes it possible to detect an antagonism by. the growth retardants of the action of either or both of these hormones. This study shows that the growth retardants interfere with the auxin metabolism but do not competitively inhibit the action of GA in Avena leaf sections. MATERIALS AND METHODS The procedure for obtaining Avena leaf sections has been detailed elsewhere (12). Briefly, 5-mm sections were cut from the base of cm long primary leaves of Avena sativa L., var. Victory, after removal of the coleoptile. The basal cut was 2mm above the node. Lots of 12 sections were placed in 25xl5-mm test tubes with 5 ml of medium. The test tubes were rotated on Rollordrum at lrpm. After 24 hr, the sections were removed, the 2 shortest sections were discarded (for discussion see 12) and the lengths of the remaining 1 sections were measured with a microscope fitted with an eyepiece.micrometer. The medium consisted of.1m phosphate buffer, ph 5.5, with growth factors added as indicated. When required, GA was added at a concentration of.1 ppm. This concentration is optimal for the elongation of these sections (12). GA and Amo-1618 were purchased from California Corporation for Biochemical Research. Phosfon D was a gift of the Virginia-Carolina Chemical Co. CCC was kindly supplied by the American Cyanamid Co. B995 and C11 were obtained from Dr. RIDDELL of the Naugatuck Chemical Co. These growth factors were used without further purification. All solutions were made up in glass-distilled water and the ph was adjusted to 5.5 before using. The plants were grown and the experiments were carried out under continuous illumination from a dim red light. RESULTS The five growth retardants were tested for their ability to inhibit the elongation of Avena leaf sections. One retardant, B995, was found to have virtually no effect on elongation at any concentration up to.3 M. The other four retardants all exerted some inhibition of growth, although the concentrations required for inhibition varied widely. Least effective as a growth inhibitor was CCC. Only at concentrations in excess of.1 M was inhibition of growth found (Fig. 1). Then both the GA-induced and endogenous growth were inhibited. At lower concentrations of CCC the growth of GA-treated sections was actually enhanced by this retardant. Elongation was stimulated \Z% by.1 M CCC. Although this promotion is slight, it is significant at the 5% level and was found in

3 SITE OF GROWTH RETARDANT ACTION 9 every experiment in which CCC was used. The retardant C11 was a slightly more effective inhibitor in this system (Fig. 2). The threshold for inhibition was at 3X1" 3 M. A 5% -r - co CCC CONCENTRATION (LOG M) Fig. 1. The effect of GCC on thej growth of -Avena leaf sections. Sections incubated for 24 hr with varying concentrations of CCC in the presence ( O ) or absence ( x ) of.1 ppm GA. u GROWTH-mm/2 6 5* *- - C> id" 6 CO11.GA Amo«GA - ^ - 16 s \ \ id 4 > PD.GA S--PD-GA \ V. 1" 3 CONCENTRATION-M Fig. 2. The effect of three retardants on Avena leaf growth. Sections incubated for 24 hr with varying concentrations of retardants ±.1 ppm GA. Curves shown are for C11+GA( O ), Amo+GA ( X ), PD+GA( A ) and PD-GA ( D ) \ \ TO 2

4 1 R. CLELAND Vol. 6 (1965) inhibition of the elongation of GA-treated sections was obtained with 3X1~ 2 M C11. No growth promotion was found with this compound. Both endogenous and GA-induced elongation were markedly inhibited by levels of Amo-1618 in excess of 3X1~ 4 M. The elongation of GA-treated sections was inhibited 5% by 2X1~ 3 M Amo-1618 (Fig. 2). Complete inhibition of growth was found at 1~ 2 M. Amo-1618 did not promote elongation at any concentration. The most effective inhibitor was Phosfon D. The threshold for inhibition was 3X1" 5 M. A 5% inhibition of the elongation of GA-treated sections was found at 2X1~*M and virtually complete inhibition was obtained at 1~ 3 M (Fig. 2). The apparent stimulation of growth by lower concentrations of Phosfon D is not significant. The inhibitory effect of Phosfon D was not constant but varied with time after application. This is shown in Fig. 3. At level of 3X1~ S M it had no effect for 4-6hr. Thereafter growth was severely inhibited. At a lower level (1"*M), Phosfon D was active only after a lag of 9-1hr. The inhibition increased until after 18 hr it was as severe as with the higher level of Phosfon D. It would appear that Phosfon D affects the duration rather than the rate of growth of Avena leaf sections. The two retardants Amo-1618 and Phosfon D possess the ability to strongly inhibit GA-induced elongation. Are these compounds acting as competitive antagonists of GA? If so, the addition of an excess of GA TIME-hr Fig. 3. Time course of effect of Phosfon D on the growth of Avena leaf sections. Sections incubated without growth factors ( A ), with.1 ppm GA ( O ), with.1 ppm GA and 1~* M PD ( x --) or with.1 ppm GA and 3 x 1- s M PD (- -)

5 SITE OF GROWTH RETARDANT ACTION 11 should at least partially reverse this inhibition. In order to test this, sections were incubated for 24 hr with varying levels of GA in the presence or absence of 1~*M Phosfon D. The resulting curves are shown in Fig. 4. In the case of competitive inhibition, the curves would be expected to converge as the GA concentration is increased (for discussion see 7). Instead, the curves were found to diverge. In the absence of the retardant, a maximal promotion of growth was obtained with.3 ppm GA. In the presence of Phosfon D, GA had only a small effect on elongation with a maximum being reached at.3 ppm. Further increases in the GA level did not lessen the effect of the Phosfon D. Similar results were obtained with Amo It is apparent that the inhibitory effect of the retardants cannot be overcome by GA. The reterdants do not act at the site of GA-action. 6" SB H o «o ,o-o - Phosphon Phosphon GA CONCENTRATION-ppm Fig. 4. Effect of GA concentration on the inhibition induced by Phosfon D. Sections incubated for 24 hr with varying levels of GA in the presence (~O~) or absence ( X ) of 1-* M Phosfon D. KURAISHI and MUIR (11) and HALEVEY (9) have suggested that the growth retardants act on some facet of the auxin metabolism of the tissue. If this is correct, the inhibition should be partially reversed by the addition of auxin. The following experiment was carried out in order to see if this occurred in Avena leaf tissues. Sections were incubated with varying levels of IAA in the presence or absence of 2X1" 4 M Phosfon D. All solutions also contained.1 ppm GA. It can be seen from Table I that the added IAA has partially reversed the inhibitory effects of the Phosfon D. The magnitude of the reversal is difficult to assess because the added auxin is

6 12 -R. CLELAND Vol. 6 (1965) TABLE I The reversibility of the Phosfon D inhibition with IAA.Phosfon D 2xlO-«M IAA ppm Growth mm/24 hr 5.29± ± ± ± ± ± ± ±.16 A 2.97 ± ± ± ±.23 % reversal Sections incubated for 24 hr with varying concentrations of IAA, either in the presence or absence of 2xlO~ 4 M Phosfon D. Initial length 5.±.3mm. slightly inhibitory to elongation (12). Similar results were obtained with Amo Thus it appears that at least part of the inhibitory action of these retardants is due to an antagonism of the auxin metabolism of this tissue. However, the fact that a part of the inhibition caused by these retardants could not be reversed by either auxin or gibberellin indicates that the retardants exert an inhibition of growth which is unrelated to the hormonal metabolism of this tissue. DISCUSSION The five compounds used in this study have been grouped together because of their ability to interact with GA in various systems. The manner in which this interaction occurs has not yet been settled. At least four possible modes of action have been proposed. Experimental evidence has been obtained to support three of these. First, growth retardants may cause inhibitions which are not directly related to either GA or auxin metabolism. SACHS and WOHLERS (14) have shown that the inhibiting effect of retardants on carrot callus growth is not reversed by either GA or auxin. Likewise, the effect of CCC and Phosfon D on the growth of Raphanus leaf discs was not reversed by either GA or auxin (11). In Avena leaf sections part of the inhibitory effects of Amo-1618 and Phosfon D were of this type. A second possibility is that growth retardants block the synthesis of GA. The ability of CCC and Amo-1618 to prevent GA synthesis mfusarium moniliforme has been shown by KENDE et al. (1). As yet it has not been shown that the retardants will cause a similar inhibition of gibberellin

7 SITE OF GROWTH RETARDANT ACTION 13 synthesis in higher plant tissue. The expected result of such an inhibition would be that the growth retardants would cause a competitive inhibition of the endogenous growth but would be without effect on the growth produced by added GA. Results consistent with this mode of action have been obtained by SACHS et al. (15), TOLBERT (16), LOCKHART (7), and CATHEY (17). This suggests that such an inhibition of GA synthesis may occur. A third possibility is that the growth retardants affect some aspect of the auxin metabolism of the tissue. There is considerable evidence to support such a mode of action in higher plants. KURAISHI and MUIR (11) found that the production of diffusible auxin by the apex of Alaska pea seedlings was severely inhibited by CCC. Treatment of cucumber seedlings with Amo-1618, CCC, Phosfon D or B995 resulted in a marked increase in the IAA-oxidase activity of hypocotyls and cotyledons (9). The auxin-induced growth of Avena coleoptile tissues is inhibited in a non-competitive manner by several, of the growth retardants. (11, 13, 18). Finally, in this study it was shown that the inhibiting effects of the growth retardants- on Avena leaf sections could be partially reversed by addition of auxin. The response of tissues to this mode of action would depend upon the relationship between auxin, gibberellin, and growth. Both competitive and; non-competitive inhibitions would be consistent with type of action. If gibberellins control growth, by regulating the level of auxin in the tissue as has been suggested by GALSTON and WARBURG (2), BBRGMANN (21), and KURAISHI and MUIR (19), the retardants should competitively inhibit both the endogenous and the GA-induced growth. Should auxin and GA not be directly interrelated, a non-competitive growth inhibition would be expected. Both competitive and non-competitive interactions between retardants and GA have been found. Finally, the growth retardants might be competing with gibberellin at the site of GA action. There is no evidence to support this idea. The results of this study show that such a competitive interaction does not occur in Avena leaf tissue. Similar results were obtained by KURAISHI and MUIR (11) with Raphanus leaf discs. PALEG has found no interaction between GA and the growth retardants in the barley endosperm test (22). TOLBERT concluded that such an interaction was unlikely on theoretical grounds (23). The apparent interaction between retardants and GA-induced growth in intact systems can be due to an effect of the retardants on GA synthesis or auxin metabolism. The question remains as to how the growth retardants exert their effect. This problem is complicated by the diversity of responses which different tissues show to the growth retardants. Many tissues are resistant to all of the retardants (24, 25). Others are affected by only one or several of these compounds. Avena. leaf tissues show marked differences in sensitivity to the various growth retardants. This difference in sensitivity is probably due to the ability of some plant to exclude or metabolize certain of the retardants.

8 14 R. CLELAND Vol. 6 (1965) Tissues differ not only in their sensitivity to the retardants but also in the type of inhibition which is produced. In certain systems there is a non-competitive interaction between GA and the retardants. Among these are the growth of dark grown cucumber hypocotyls (6), Avena coleoptile sections (11, 13, 18) and the germination of lettuce seeds (18). In other systems competitive interaction between the growth retardants and GAregulated systems has been demonstrated. These include the growth of Alaska pea stems (7), Thatcher wheat stems (16), Phaseolus vulgaris hypocotyls (26), and both growth (17) and cell division in the subapical meristem of Chrysanthemums (15, 27). It is clear that the retardants act on the endogenous growth. The relationship of the retardants to added GA is less certain. Clearly added GA will reverse the inhibitory effects of the retardants but it has not yet been conclusively shown that the growth retardants will reverse the effects of added GA. The results of LOCKHART (7) and DOWNS and CATHEY (26) suggest that this may occur but further experiments on this matter will be needed. From the diversity of responses of tissues to retardants, one must conclude that these compounds possess more than one mode of action. Tissues appear to differ in that they may be susceptible to one, more than one or none of these modes of action. In the Avena leaf, the growth retardants appear to act both by interfering with the auxin metabolism of the tissue and by exerting an inhibition of some non-hormonal aspect of growth. REFERENCES ( 1 ) H. M. CATHEY Physiology of growth retarding chemicals. Ann. Rev. Plant Physiol., 15, ( 2 ) J. W. WlRWILLE and J. W. MITCHELL Six new plant-growth inhibiting compounds. Bot. Gaz., Ill, ( 3 ) N. E. TOLBERT Chloroethyltrimethylammonium chloride and related compounds as plant growth substances. I. Chemical structure and bioassay. J. Biol. Chem., 235, ( 4 ) W. H. PRESTON and C. B. LINK Use of 2,4-dichlorobenzyl tributylphosphonium chloride to dwarf plants. Plant Physiol., 33, xlix. ( 5 ) J. A. RIDDELL, H. A. HAGEMAN, C. M. J'ANTHONY and W. L. HUBBARD Retardation of plant growth by a group of chemicals. Science, 136, 391. ( 6 ) A. H. HALEVEY Interaction between gibberellin and quaternary ammonium carbamates in growth of cucumber seedlings. Bull. Res. Counc. Israel, 11D, ( 7 ) J. A. LOCKHART Kinetic studies of certain antigibberellins. Plant Physiol., 37, ( 8 ) J. A. D. ZEEVAART and A. LANG Suppression of floral induction in Bryophyllum daigremontianum by a growth retardant. Planta, 59, ( 9 ) A. H. HALEVEY Interaction of growth retarding compounds and gibberellin on indoleacetic acid oxidase and peroxidase of cucumber seedlings. Plant Physiol., 38,

9 SITE OF GROWTH RETARDANT ACTION 15 (1) H. KENDE, H. NlNNEMANN and A. LANG Inhibition of gibberellic acid biosynthesis in Fusarium moniliforme by Amo-1618 and CCC. Naturwiss-, 5, (11) S. KURAISHI and R. M. MUIR Mode of action of growth retarding chemicals. Plant Physiol., 35, (12) R. CLELAND The role of endogenous auxin in the elongation of Avena leaf sections. Physiol. Plant., 17, (13) R. CLELAND. Unpublished data. (14) R. M. SACHS and M. A. WoHLERS Inhibition of cell proliferation and expansion in vitro by three stem growth retardants. Am. J. Bot., 51, (15) R. M. SACHS, A. LANG, C. F. BRETZ and J. ROACH Shoot histogenesis: Subapical meristematic activity in a caulescent plant and the action of gibberellic acid and Amo ibid., 47, (16) N. E. TOLBERT Chloroethyltrimethylammonium chloride and related compounds as plant growth substances. II. Effects on growth of wheat. Plant Physiol., 35, (17) H. M. CATHEY Effects of gibberellin and Amo-1618 on growth and flowering in Chrysanthemum morifolium on short photoperiods. In Photoperiodism and Related Phenomena in Plants and Animals. Edited by R. B. WlTHROW. p AAAS, Washington, D. C. (18) S. H. WITTWER and N. E. TOLBERT Chloroethyltrimethylammonium chloride and related compounds as plant growth substances. V. Growth, flowering, and fruiting responses as related to those induced by auxin and gibberellin. Plant Physiol, 35, (19) S. KURAISHI and R. M. MUIR Increase in diffusible auxin afer treatment with gibberellin. Science, 137, (2) A. W. GALSTON and H. WARBURG An analysis of auxin-gibberellin interaction in pea stem tissues. Plant Physiol., 34, (21) L. BERGMANN Der Einfluss von Gibberellin auf das Wachstum von Gewebekulturen des Callus von Daucus carota. Planta, 51, (22) L. G. PALEG. Personal communication. (23) N. E. TOLBERT Structural relationships among chemicals which act like antigibberellins. In Gibberellins. Edited by R. F. GOULD, p Amer. Chem. Soc, Washington, D. C. (24) P. C. MARTH, W. H. PRESTON, JR. and J. W. MITCHELL Growth-controlling effects of some quaternary ammonium compounds on various species of plants. Bot. Gaz., 115, (25) H. M. CATHEY and N. W. STUART Comparative plant growth-retarding activity of Amo-1618, Phosphon and CCC. ibid., 123, (26) R. J. DOWNS and H. M. CATHEY Effect of light, gibberellin and a quaternary ammonium compound on the growth of dark-grown red kidney beans, ibid., 121, (27) R. M. SACHS and A. M. KOFRANEK Comparative cytohistological studies on inhibition and promotion of stem growth in Chrysanthemum morifolium. Am- J. Bot., 5,

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