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1 The Ohio State University, Department of Plant Biology, Columbus, Ohio 43210 USA
Received for publication March 16, 1999. Accepted for publication June 11, 1999.
ABSTRACT
The classic Thimann-Skoog or auxin replacement apical dominance test of exogenous auxin repression of lateral bud outgrowth was successfully executed in both seedlings and older trees of white ash, green ash, and red oak under the following conditions: (1) decapitation of a twig apex and auxin replacement were carried out during spring flush, (2) the decapitation was in the previous season's overwintered wood, and (3) the point of decapitation was below the upper large irrepressible lateral buds but above the lower repressible lateral buds. Although it has been suggested that neither auxin, the terminal bud, nor apical dominance have control over the outgrowth of the irrepressible buds during spring flush, there is evidence in the present study that indicates that such control over the repressible buds exists. In seedlings, second-order branching, which resulted from decapitation of elongating current shoots, was also inhibited by exogenous auxin in the three species. Hence, the auxin replacement experiments did work on year-old proleptic buds (of branches of older trees) that would have entered the bud bank and also on current buds of seedlings. Cytokinin treatments were ineffectual in promoting bud growth.
Key Words: apical dominance • auxin • decapitation • Fraxinus americana • Fraxinus pennsylvanica • lateral bud growth • Quercus rubra.
Apical dominance is the control exerted by the shoot apex over the outgrowth of the lateral buds. In 1933 Thimann and Skoog removed the shoot apex of the herbaceous species Vicia faba and repressed subsequent lateral bud outgrowth by application of auxin to the top of the decapitated stem. This classical auxin replacement experiment, which works in many herbaceous plants (Tamas, 1995
; Cline, 1996
), is commonly cited as evidence for a repressive role of apically produced auxin in the control of lateral bud growth in apical dominance. Subsequent studies also have suggested an interaction of cytokinin with auxin in bud growth (Sachs and Thimann, 1967
).
Because of substantial evidence (e.g., forking in shoots following injury to terminal buds) for apical dominance in woody plants, models of apical dominance employed for herbaceous plants are generally used to explain apical dominance in these plants as well. This extrapolation is done in spite of the recognition of the significantly increased morphological and physiological complexity of woody species with respect to such factors as perennial growth habits, the predominance of woody vascular tissue, and endodormancy.
The way that these herbaceous models may be applied to trees has been considered by a number of authors. Brown, Alpine, and Kormanik (1967)
have pointed out that the term "apical dominance" as used for herbaceous plants by Thimann and Skoog should not be employed for a whole tree but only for the current year's growth. Similarly, Wareing (1970)
has explained that it would be difficult to envision auxin moving down a considerable distance from the main shoot apex and then acropetally far out to the apices of branches to control lateral bud growth. Sundberg and Uggla (1998)
have also pointed out that in tall trees with the slow rate of polar auxin transport (e.g., 1 cm/h), it takes months for an auxin molecule to move down the trunk from the tip. This complicates the explanation of apical control by auxin. Other workers (Romberger, 1963
; Tomlinson and Gill, 1973
; Timell, 1986
; Wilson, 1990
; Bollmark et al., 1995
) have also recognized the difficulty of explaining the mechanism of auxin control of apical dominance at the whole-tree level.
To what degree can we expect the auxin replacement experiment, which works so well with most herbaceous plants, to be applicable to trees in the field? Although it may be presumed that the response in the current year's growth of woody plants is similar to that in herbaceous plants, such studies are lacking on intact branches of trees, particularly of trees beyond the seedling stage. Many of the reports involve in vitro systems, stem cuttings, and indirect approaches.
Gunckel, Thimann, and Wetmore (1949)
demonstrated that 1% NAA (naphthaleneacetic acid) applied to the cut surface of decapitated 3-yr-old Ginkgo seedlings inhibited short lateral shoots from growing into long lateral shoots. However, since the short laterals have already grown out to some extent it could be argued that this is not a clear case of repression of apical dominance release but rather one of subsequent apical control (Cline, 1997
). Similarly, after removing all the laterals except the longest in the whorl of white pine saplings, Little (1969)
treated the decapitated terminal with auxin (5–20 mg/g) and observed the prevention of a small amount of compensatory growth in the remaining lateral, which was interpreted in terms of auxin-directed nutrient diversion. Wang, Faust, and Line (1994)
found that IAA (indoleactic acid, 10–100 nmol) injected into the decapitated tips of 25-cm-long excised apple shoots collected in August and placed in glass jars containing distilled water repressed the growth of the most distal lateral buds. Yang and Read (1991)
in their in vitro culture experiments have found a reduction in the percentage of privet bud break and shoot elongation when IAA or NAA was added.
Wignall and Browning (1988)
have reported NAA (20 mg/dm) inhibition and BA (benzyladenine, 20 mg/dm) reversal of this inhibition of epicormic bud development in stem explants of Quercus robur over a 6-wk period. Leaky and Longman (1986)
found a 85–35% reduction in actively growing buds in rooting stem cuttings of Triplochiton scleroxylon with 250-µg NAA injections; 1 mg BA had no effect. Wilson (1979)
reported that IBA (indolebutyric acid 10-4 M) totally inhibited epicormic bud growth in decapitated stem segments of Acer pennsylvanicum L., whereas GA (gibberellic acid) and BA had no effect on initial bud release. Bowersox and Ward (1968)
found NAA, IBA, and IAA to equally inhibit epicormic branching in white oak stem segments. Recently, House et al. (1998)
reported that auxin (NAA, IBA, IAA, and 2,4-dichlorophenoxyacetic acid, 10–0.01%) applications in lanolin to exposed cut surfaces of 3-yr-old hoop pine (Araucaria cunninghamii) stocks could temporarily repress the outgrowth of orthotropic replacement shoots.
The objective of the present study was to determine whether the auxin replacement experiment would work on seedlings and on intact branches of older trees (green ash, white ash, and red oak) and to elucidate the role of auxin in apical dominance in these woody species. These three species are ring-porous with a fixed growth period in mid-spring and were selected because of their vigorous shoot growth. Cytokinin (BA) effects were also analyzed.
MATERIALS AND METHODS
For the greenhouse seedling studies, 100 seedlings (beginning their second year) of white ash (Fraxinus americana var. americana L.), green ash [Fraxinus pennsylvanica var. subintegerrima (Vahl.) Fern], and red oak (Quercus rubra L.) were obtained (bare root) from the outside plantings of the Ohio Division of Forestry nursery at Zanesville in late March 1996 and were planted in (3.8 L, one gallon) pots containing Pro-mix, a general-purpose peat-vermiculite growing medium on 2 April and placed in a greenhouse (16°–32° C) with supplementary General Electric 400-W mercury vapor lamps (total irradiance up to 3300 µmol·m-2 s-1).
The first of three white ash seedling experiments involving decapitation, 1% IAA (~60 mmol/L) or NAA (~45 mmol/L) in lanolin and 100–200 mg/L (444–889 mmol/L) BA spray treatments (5–10 plants each) was begun 9 April as the buds were beginning to grow out. The IAA, NAA, and BA were obtained from Sigma Chemical Co., (St. Louis, Missouri, USA). IAA was dissolved in warm alcohol before mixing with hot lanolin. The BA in powder form was dissolved in water with glacial acetic acid. BA in solution (1 mg/mL) obtained from Sigma was also used. The stems were decapitated ~0.5 cm above the fourth node down from the terminal bud, and auxin was immediately applied to the top of the stump of the decapitated stem. The BA spray was applied to the shoot at least once a week for 2–3 wk. The concentration of the BA was increased from 444 to 889 mmol/L (pH 7.2) for the last two treatments to increase the likelihood of a a response. The seedlings for the second-order branching experiment were taken from the decapitated controls of these three white ash experiments. The two growing highest lateral shoots (resulting from previous decapitation) were themselves decapitated 7 May below the terminal bud (see Fig. 2). One was treated with lanolin and the other was treated with auxin (1% IAA or NAA) in lanolin. Determinations were then made of second order outgrowth of the next two lower lateral buds on each of the two shoots. The first of two green ash experiments were begun on 18 April and carried out as with those of white ash.
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For the 1996 tree field studies, the following selections were made: nine white ash (~15-yr-old), four green ash and four red oak trees, both 5- to 6-yr-old. The selections were made before bud break had occurred. As it turned out, all the white ash were vigorous healthy trees. However, a few of the green ash and red oak trees had some dead and unhealthy branches. Data from these latter branches were included in the averaged data.
The white ash decapitation and auxin treatments were begun on 20 April, coinciding with the beginning of spring flush and floral bud opening, which preceded that of the vegetative buds. For these field studies the more persistent auxin, NAA, was used instead of IAA. Decapitation was carried out above the second or third node below the terminal bud on a twig of at least three or four nodes, thus leaving buds located on the lower nodes for possible sprouting (see Fig. 4). One percent NAA in lanolin was immediately applied to the stump of specific decapitated twigs. Final measurements were made on 19 August. No BA treatments were given.
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The red oak decapitation and NAA treatments in the field were begun on 29 April as buds were beginning to sprout with a variable decapitation point partway down the 1995 growth wood just above medium- to small-size lateral buds. Irrepressible large lateral buds were manually removed. On the following day, 30 April, more twigs were decapitated, this time in the pre-1995 wood, i.e., the 1994 or even 1993 wood just above any persistent medium- to small-sized lateral buds. Measurements were made on 16 May and 22 August. BA spray treatments were given to select intact shoots as described for green ash.
RESULTS
Greenhouse studies of seedlings
White ash
Overwintered seedlings with a mean height of 39.2 ± 6.9 cm (N = 8) were brought into the greenhouse on 2 April. Lateral buds began to grow within a week, at which time treatments were applied. In a majority of the intact seedlings lateral bud growth occurred at the upper nodes. Decapitation at any location on the stem released lateral buds at the node below the point of decapitation (Table 1). Stems were decapitated in early and mid-April (as the terminal buds were beginning to grow out) above the fourth node down from the terminal bud (Fig. 1). The relatively few large lateral buds that were present on the upper portion of intact stems generally grew out without decapitation. The application of IAA in lanolin on the stem following decapitation resulted in the strong inhibition of growth of the lower and smaller lateral buds. Periodic spray treatments with cytokinin (BA) to the intact shoots had no promotive effect on the lateral buds, but a moderately toxic wrinkling effect was observed on the leaves. The main stem elongated 28.3 ± 6.4 cm (N = 8) during the 1996 growing season.
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Red oak
The main stems of the red oak seedlings were leaning and not as straight and upright as those of the ashes. The mean initial height was 40.7 ± 7.6 cm (N = 8). Distribution of the lateral buds, heterogenous in size, on the stem is alternate and is not uniform as compared to that of the ashes. Near the stem apex, there was often an unsymmetrical cluster of buds. Although there was more sprouting on the upper portion of the shoot than lower down, it was not unusual to observe a large growing lateral bud lower down. These large buds were manually removed since they would have grown out anyway, having little or no sensitivity to exogenous auxin treatment at this late stage of development. Decapitation released lateral buds high on the stem and close to the point of decapitation. The inhibitory effect of the NAA treatment on lateral bud growth was marginal (Fig. 1, Table 1). The main stems elongated 9.8 + 4.2 cm (N = 8) during the growing season. Second-order outgrowth, repressible by auxin (Table 2), was also observed in red oak. No BA effects were seen.
Field studies with trees
White ash
There were some significant differences in the responses between the stems of the greenhouse seedlings and the twigs on the branches of the 15-yr-old outdoor trees during 1996. The twigs of the latter were oriented in a more or less horizontal position, whereas the stems of the greenhouse seedlings were upright. Stems of the greenhouse seedlings averaged 40 cm with ten nodes, whereas the 1995 wood of the older tree branches averaged 16 cm with three or four nodes in the terminal shoots and two or three nodes in the side shoots. Another obvious difference was the widespread presence of floral buds in the older trees.
The terminal bud was always vegetative and always grew out if present (Fig. 3). Laterally adjacent to the terminal bud are two axillary buds, which often do not grow out (Gill, 1971
). Nearly half of the axillary buds at the first node below the terminal bud were vegetative and did grow out (data not shown). Many of the buds at the second and third nodes down were floral. Within a few weeks after sprouting, the floral shoots on all of the nine trees except one had abscised. Likewise, all external latent buds eventually appeared to have abscised so that at the end of the 1996 growing season, the only visible appendages left on the 1996 wood were vegetative shoots at the terminal position and at some of the upper nodes.
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There was an average of 1.8 lateral buds left on the twig after decapitation and of these 1.5 sprouted (Table 4). This 83% outgrowth following decapitation was certainly greater than the 23% sprouting that normally occurred in the intact stems and strongly suggests that apical dominance was released by decapitation. Decapitation-induced release of apical dominance was strongly inhibited by auxin (Table 4). Large swelling buds below the point of decapitation were manually removed. The percentage of sprouting lateral buds was much higher in terminal stems than in side stems. When 1% NAA was applied to decapitated terminal stems that still had many large lateral buds on the verge of sprouting, the inhibitory and somewhat toxic effect of the NAA was limited to the topmost one or two lateral buds only 1–2 cm from the site of NAA application, whereas the remaining large lateral buds, lower on the shoot, appeared to sprout normally (data not shown). BA spray had no effects.
DISCUSSION
In all three species, both with seedlings and with older trees, decapitation induced growth of the repressible buds, which in white ash also included the bud-scale buds (Fig. 5) at the base of the 1995 wood. These releases were repressible by auxin application to the decapitated shoot in all cases except for red oak seedlings where the repression was negligible. Perhaps the considerable distance between the site of auxin application and the positions of some of the widely scattered lateral buds prevented the response. Second-order branching after decapitation of the first-order branches, repressible by exogenous auxin, was observed in the seedlings to some degree in all three species (Fig. 2). In contrast to the cytokinin-promotive effects that a number of investigators have found (Williams and Stahly, 1968
; Yang and Read, 1991
), no BA enhancement effect was observed on lateral bud growth here.
This investigation has clearly elucidated some significant differences between the execution of the auxin replacement experiment with herbaceous vs. woody species. Decapitation of a vigorously growing herbaceous plant with relatively strong apical dominance such as pea will at any time almost immediately trigger the initiation of the outgrowth of some of the lower lateral buds (Stafstrom, 1995
; Cline, 1996
). This release of apical dominance can be repressed by the application of auxin on the stump of the decapitated stem. However, with the three woody species studied here, the time of the execution of the experiment was essentially restricted to spring flush.
Auxin replacement experiments cannot be done if decapitation does not release the lateral buds in the controls. Rapid bud growth such as occurs during the flush period provides optimal conditions for the detection of auxin repression in decapitated shoots. This is particularly true for older trees in field conditions. In the present study, decapitation of the shoot apex during this period usually released the lateral buds within a week or so (data not shown), and the repressive effects of applied auxin could be clearly observed. If the bud release in the decapitated control shoots is slow, i.e., over a period of many weeks or months, then it is possible that complicating physiological and environmental factors may obscure the interpretation of the auxin effects. When white ash shoots were decapitated later in the growing season, the outgrowth of the lateral buds was very limited (data not shown) and unsuitable for auxin replacement experiments.
There are two further restrictions. The first is that the decapitation must be made in the previous season's overwintered growth wood except for seedlings. It is reported elsewhere (Cline and Deppong, 1999
) for these three species (in older trees) that decapitation in the present season's growth wood during the flush period does not release the current lateral buds, suggesting the existence of some inhibitory influence other than apical dominance. The second restriction is that the point of decapitation must be below the larger upper irrepressible lateral buds, which grow out synchronously with the terminal bud during the spring flush, and above the smaller, lower repressible buds, which will not grow out without decapitation (Fig. 4). These latter proleptic buds were those that responded to the auxin replacement test. Whether auxin is the natural repressor of these latent buds remains to be confirmed, but the evidence is suggestive.
Since the large upper irrepressible lateral buds exhibit little or no inhibition in their vigorous outgrowth during spring flush, it was deemed unfruitful to attempt auxin replacement experiments to test auxin inhibitory effects in these buds. As mentioned in the Results section with older red oaks, exogenous auxin had little effect on these large buds (data not shown). Brown (1970)
has pointed out that the larger upper irrepressible lateral buds of woody plants are not under auxin inhibition of the terminal bud nor under the control of apical dominance during flushing. However, this is not to say that there may not be, under certain conditions, some kind of apical control by the elongating terminal bud in the subsequent outgrowth of these irrepressible lateral buds. The occasional lack of such control in summer flushing of douglas-fir appears to cause an anomalous branching and forking response in the shoot apex.
The lack of uniformity observed here in the bud distribution of red oak and the fact that some buds were damaged or missing has also been reported by other workers (Ward, 1964
; Harmer, 1991
). Harmer points out that in Quercus petraea the buds are spirally arranged with the pitch of the spiral being much smaller near the shoot apex with greatly increased bud density. Likewise the fact that decapitation was followed by the outgrowth of lateral buds closest to the cutting point was also found by Wilson and Kelty in black oak (1994). Furthermore, their finding that the removal of all large buds in black oak enhanced the outgrowth of epicormic buds also was supported in the present study with red oak, although a separation between normal lateral and epicormic shoots was not made. NAA inhibited the outgrowth of both kinds of shoots. Similarly, in the present study of red oaks, decapitation (and removal of large buds) released 94% of the remaining lower buds. Many of the lateral buds abscised. Harmer and Baker (1995)
determined that decapitation of terminal buds in Quercus petraea was most effective in promoting branching when carried out during the second flush.
Remphrey and Davidson (1992)
have pointed out that the outgrowth of epicormic shoots is often thought to be due to the sudden exposure to light because of pruning or thinning and the subsequent photodestruction of auxin. They further indicate that the work of Wignall and Browning (1988) suggests that it is not the decrease in auxin but the counteractive effect of cytokinin on auxin that promotes outgrowth. However, as Remphrey and Davidson (1992)
explain, the pruning and thinning may simply result in a larger supply of nutrients, water, and cytokinin, which promote the outgrowth. Auxin replacement studies with apical dominance in herbaceous plants suggest indirect auxin action with cytokinin effects (Cline, 1994
; Cline, Wessel, and Iwamura, 1997
).
As far as can be determined, the present study provides the first report of an apical dominance auxin replacement experiment having been carried out on the stem of an intact branch of a hardwood tree. Although the experiment was made to work in white ash, green ash, and red oak under the particular noted conditions, the foregoing results and interpretation of data do not necessarily apply universally, given the wide spectrum of physiological responses present in different woody species under different growing conditions (Brown and Sommer, 1992
).
The results of these auxin replacement experiments on intact trees generally agree with those on excised shoots reported in the literature. Where apical dominance occurs in normal development, auxin plays a primary role. However, in spite of the considerable research which has been done on the production, content, and transport of endogenous auxin in woody tissues, its precise role in apical dominance has yet to be elucidated (Wareing and Saunders, 1971
; Rinne, Tuominen, and Sundberg, 1993
; Tuominen et al., 1995
). Although the use of the auxin replacement experiment with woody plants has certain limitations, it is still a powerful tool for investigating the role of auxin in apical dominance and has generated much valuable data for providing a framework for physiological, genetic, and molecular studies of the involved mechanisms.
FOOTNOTES
1 The author thanks Drs. D. Struve, M. Larson, B. Wilson, and R. Harmer for their helpful input as well as to Ms. Cathy Maupin, Superintendent of Building and Grounds at the Ohio State University for the use of selected trees. 
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———. 1997 Concepts and terminology of apical dominance. American Journal of Botany 84: 1064–1069. [Abstract]
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Wignall, T., and G. Browning. 1988 Epicormic bud development in Quercus robur L. Studies of endogenous IAA, ABA, IAA polar transport and water potential in cambial tissues and effects of exogenous hormones on bud outgrowth from stem explants. Journal of Experimental Botany 39: 1667–1668.
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