Am. J. Bot. Join the BSA
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
QUICK SEARCH:   [advanced]


     

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Submit a response
Right arrow Alert me when this article is cited
Right arrow Alert me when eLetters are posted
Right arrow Alert me if a correction is posted
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Cline, M. G.
Right arrow Articles by Sadeski, K.
Right arrow Search for Related Content
PubMed
Right arrow Articles by Cline, M. G.
Right arrow Articles by Sadeski, K.
Agricola
Right arrow Articles by Cline, M. G.
Right arrow Articles by Sadeski, K.
(American Journal of Botany. 2002;89:1764-1771.)
© 2002 Botanical Society of America, Inc.

Physiology and Development

Is auxin the repressor signal of branch growth in apical control?1

Morris G. Cline2 and Kevin Sadeski

Ohio State University, Department of Plant Biology, Columbus, Ohio 43210 USA

Received for publication November 20, 2001. Accepted for publication June 11, 2002.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
"Apical control" is the repression of branch growth by a higher dominating branch or shoot. There has been some confusion in the literature concerning the meaning and causal mechanisms of this correlative phenomenon with those of "apical dominance," which term is often used in a strict sense to connote the repression of the initiation of axillary bud outgrowth by an active shoot apex. Although the term "apical control" is most commonly employed with respect to woody species, this phenomenon also widely occurs in herbaceous plants. Because of the strong evidence for a role of auxin as a repressor signal in apical dominance and partly because of this lack of distinction in terminology, a similar role for auxin in apical control is often assumed in spite of the obvious acropetal auxin transport difficulty and the lack of direct evidence for the acropetal transport of any inhibitor influence. In the present study with the herbaceous Ipomoea nil, it has been clearly demonstrated that while exogenous auxin (1% NAA) strongly restores apical dominance in the Thimann-Skoog experiment, auxin treatments to decapitated dominant shoots do not, in any observable way, restore apical control in lower dominated branches. Hence, in this fast-growing species, the hypothesis for the role of auxin as a repressor signal for apical control is not supported.

Key Words: acropetal auxin transport • apical control • apical dominance • auxin • branch growth • Convolvulaceae • decapitation • Ipomoea nil • lateral bud


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
"Apical control" refers to the suppression of existing branch growth imposed by the growth of a higher dominating branch or shoot (Leakey and Longman, 1986 ; Suzuki, 1990 ; Wilson, 1990 , 2000 ). This phenomenon can be clearly demonstrated by decapitating or removing the higher dominant branch or shoot. This often results in a dramatic acceleration of growth in the lower dominated branch. Before decapitation, the higher branch, in some way, controlled and repressed the growth of the lower shoot.

Recognizing the complexity of perennial branching in woody species and the inapplicability of the term "apical dominance" as used for herbaceous plants, Brown, Alpine, and Kormanik (1967) introduced the term "apical control" to describe the influence of apical portions of a tree crown over perennial branching and general tree form. Suzuki (1990) distinguishes between apical dominance and apical control in that the former refers to "correlative inhibition of axillary buds on shoots of the current year" (p. 350) while the latter refers to the "control of branches once they are growing" (p. 351). Similarly Wilson (1990) states, "apical dominance refers to whether lateral buds grow out and apical control refers to the relative length and orientation of the lateral axes that do grow out" (p. 53). Suzuki goes on to point out that control of elongation and diameter growth (as in apical control) is one step removed from inhibition of bud outgrowth (as in apical dominance). Wilson's recent (2000) comprehensive review of apical control in woody plants explores and elucidates various aspects of this phenomenon including dormancy, radial growth, and shoot angle.

In spite of these clearly articulated differences between the meanings of the terms "apical control" and "apical dominance," some workers still employ the terms interchangeably, which tends to blur the distinction between the two phenomena and their causal mechanisms. Brown, Alpine, and Kormanik (1967) , Wareing (1970) , and Timell (1986) emphasize that the term "apical dominance," as used for herbaceous plants by Thimann and Skoog (1933) to connote the control exerted by the shoot apex over the outgrowth of lateral buds, should not be employed with respect to branching in trees beyond the current year's growth.

Although the term "apical control" has most commonly been used with respect to branching in woody species (e.g., Cook, Rabe, and Jacobs, 1999 ), the phenomenon is also widely existent in non-perennial herbaceous plants. In 1934, Thimann and Skoog noted in Vicia faba "...when the longer bud was cut off, the shorter bud at once showed a noticeable increase in the rate of growth" and they concluded that "one developing bud inhibits another" (p. 331). In 1937 Snow pointed out that "...in certain circumstances the growth of not only buds but also of quite long shoots of pea and bean plants ... can be inhibited by other growing shoots" (p. 284). Saks and Ilan (1984) have reported on apical control in cotyledon growth in Helianthus while Stirk, Aken, and van Staden (1997) have studied apical control in filamentous red algae, Ceramuaceae, Rhodophyta. Other workers, Sachs (1966) , Morris (1977) , and Li and Bangerth (1999) , employing two-cotyledon shoot pea plants with one shoot dominating the other, have carried out apical control (as defined above) experiments. They have referred to this control as "correlative senescence inducing influence," "correlative inhibition," and "correlative dominance," respectively.

Because the classic Thimann-Skoog (1933) experiment, wherein the treatment of the cut stem surface with exogenous auxin represses the subsequent axillary bud outgrowth, suggests a strong direct or indirect role for apically derived auxin as the repressive signal for apical dominance, it has been natural to extrapolate this role of auxin for all correlative phenomena, including apical control. Accordingly it has been suggested that apically derived auxin from the dominating shoot moves down to the main stem and then is transported over to the dominated shoot and up to its growing region where growth is repressed.

Sachs (1966) carried out his above-mentioned study with two-shoot plants in an attempt to determine whether there were any differences in the mechanisms responsible for apical control (as defined here) and apical dominance. He reported that exogenous indoleacetic acid (IAA) (applied to the cut stem surface of the decapitated dominant shoot) partially replaced the intact dominant shoot in causing senescence of the inhibited shoot and pointed out that other factors were also involved. He concluded that there was a general similarity between correlative phenomena of the two processes. Morris (1977) has presented data consistent with these results in the same two-shoot system. Although he found that the removal of the dominant shoot restored the capacity of the subordinate shoot to transport apically-applied (14C) IAA, he did not detect any (14C) IAA being taken up by the dominated shoot when it was applied to the dominant shoot. Li and Bangerth (1999) likewise found no movement of labeled IAA to the dominated shoot but from general evidence they concluded that correlative inhibition between the two branches is comparable to the regulating mechanism of apical dominance.

Saks and Ilan (1984) found IAA added to the cut stem surface of Helianthus did move into the existing cotyledons and did partially inhibit their decapitation-promoted growth. They concluded that the apical region of the stem controls the development of lateral organs and that auxin is most probably an important component of this system. Although these data appear to support the auxin repressor hypothesis for apical control of cotyledons, there is a question as to the degree of physiological similarity between cotyledons, which are unique senescing storage organs on the one hand, and indeterminate branches on the other hand, which have the potential for extensive growth.

Snow (1931 , 1937 ), who first developed the two-shoot system in Vicia faba, used it to demonstrate that apical dominance was controlled by an inhibitory influence, which moved down one shoot and up the second shoot where the lateral bud was located. As long as the first shoot was vigorously growing, the lateral bud on the second shoot (decapitated) exhibited little or no outgrowth. However, if the first shoot also were decapitated, then the lateral bud on the second shoot grew out. Snow interpreted these results to indicate that although auxin might well be the inhibitory influence moving down the first shoot, it could not be the inhibitory influence moving up the second shoot to the lateral bud because auxin is not known to be transported acropetally. Presumably, there would have to be some acropetally moving secondary inhibitor responsible for this. He applied this same line of thinking to apical dominance in a single shoot, i.e., apically derived auxin, having moved basipetally down the shoot, could not then move acropetally from this shoot up into an axillary bud and inhibit it. Hence, Snow rejected the "direct theory" of auxin action in apical dominance. Rather he supported an "indirect theory," which involved auxin-enhanced production or activation of a secondary inhibiting influence (capable of acropetal transport) that prevented bud outgrowth. In Snow's (1937) own words: "the inhibitory influence can travel where auxin cannot travel" (p. 290). As far as can be determined, Snow never actually carried out any exogenous auxin treatments in this two-shoot system.

Snow (1937) also observed a release of apical control in his two-shoot system following the removal of the dominant shoot, which resulted in "unchecked" growth of the previously dominated shoot. Presumably he would attribute the expression of this apical control in the dominated shoot directly to an unidentified acropetally transported "secondary inhibiting influence" and only indirectly to auxin, which might play some kind of antecedent role. He was of the opinion that correlative inhibition in buds and in growing shoots was the same.

Although there is similarity between apical dominance and apical control (as defined above and excluding perennial growth ramifications) with respect to the fact that in both cases an upper growing shoot exerts control over the growth of a lower shoot organ, there is question as to the precise role of auxin in each of these processes, if any. In the classic Thimann-Skoog apical dominance experiment (1933) , it is widely recognized that exogenous auxin treatment to the cut stem surface is very effective in repressing subsequent lateral bud outgrowth in most herbaceous species and strongly suggests at least an indirect role for auxin as a repressor signal in apical dominance (Cline, 1994 , 1996 ). This involves downward basipetal auxin transport in the main shoot and possibly the acropetal transport of auxin or some secondary inhibitor for a short distance into the axillary bud. Thus far there is little evidence to support the existence of this latter process or for direct auxin inhibition of lateral bud outgrowth in apical dominance. The role of auxin in apical dominance appears to be indirect and may well involve the action of other hormones (including cytokinins from the roots), signals, and/or nutrients (Cline, 1994 , 1996 ; Napoli, Beveridge, and Snowden, 1999 ; Shimizu-Sato and Mori, 2001 ).

There has been legitimate concern about the high concentration of exogenous auxin (1%, ~6 x 10–2 mol) needed for the successful execution of the Thimann-Skoog apical dominance experiment. Thimann and Skoog (1933) state: "The necessity for applying larger amounts of growth substance than can be obtained from the terminal bud is fully justified on the ground that the application is generalized over the whole stem surface, while the normal supply from the tip is localized in the conducting tissue and therefore more effective in its action" (p. 716). They also report that following the removal of exogenous auxin from the cut stem surface, normal bud outgrowth resumes, indicating no toxic effects of the auxin treatment on the plant. Stafstrom and Sussex (1992) found that bud growth on cultured pea cells could be inhibited completely by 10–5 mol IAA, a physiological concentration of auxin.

The acropetal transport problem (particularly for auxin) is exacerbated in apical control (Wilson, 1990 ) because of the necessity of inhibitor transport up through the entire length of the dominated branch in order for repression of tip growth. As indicated above, some workers (Sachs, 1966 ; Morris, 1977 ; Li and Bangerth, 1999 ) have reported partial restoration effects of apical control by exogenous auxin treatments of decapitated dominant shoots even though no evidence has been found of auxin movement into the dominated shoot. Gunckel, Thimann, and Wetmore (1949) reported on what appears to be a type of apical control study on 3-yr-old Ginkgo seedlings. They found that 1% NAA (naphthaleneacetic acid) applied to the cut stem surface inhibited short lateral shoots from growing into long shoots. Similarly, Little (1969) found an inhibition of a small amount of compensatory growth in a remaining lateral shoot in white pine saplings after treating the decapitated terminal with auxin (5–20 mg/g) following the removal of all laterals except one in a whorl.

Over the years we have carried out extensive tests on auxin effects on apical dominance with Ipomoea nil, Japanese morning glory (Prasad, Hosokawa, and Cline, 1989 ; Hosokawa et al., 1990 ; Prasad et al., 1993 ; Cline, 1996 , 2000 ; Cline, Wessel, and Iwamura, 1997 ). This species grows vigorously, with elongation rates of up to 10–12 cm/d and is very sensitive to auxin repression (particularly to NAA) in the Thimann-Skoog test. Our purpose in the present study has been to reduce apical control to its simplest system (of a higher dominating branch or shoot repressing the growth of a lower dominated branch without regard to perennial branching) in this herbaceous species. Although the involvement of branch orientation, diameter growth, and dormancy/perennial responses in apical control are very significant in many woody species, they will not be considered here. Hence, the scope of this study entails only one aspect of apical control and perhaps the most important—branch elongation during one season of growth.

Our objective has been to test the auxin repressor hypothesis for apical control by carrying out a variety of experiments involving exogenous auxin treatments to the stumps of the upper dominant branches or shoots following their decapitation or removal and to compare their inhibitory effects on apical dominance and apical control. Is exogenous auxin as effective in restoring apical control in Ipomoea nil as it is in restoring apical dominance? Attempts have been made with Ipomeoa nil to repeat those two-cotyledon pea shoot experiments carried by other workers as previously described. What, if any role, does auxin play in apical control of Ipomoea branching? Are there any implications of these results for woody species?


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 LITERATURE CITED
 
Seeds of Ipomoea nil L. Roth, strain violet (syn. Pharbitis nil) (Japanese morning glory) from Marutane, Kyoto, Japan, were scarified in concentrated sulfuric acid for 35 min and soaked in running water overnight before germination in petri dishes for several days. The germinating seedlings were then planted in Pro-mix (Premier Hortitculture, Red Hill, Pennsylvania, USA), a general purpose peat-vermiculite growing medium, in 10.2 cm pots. The plants from which data are presented were maintained in a vegetative condition in a greenhouse (25°–28°C) under continuous light with supplementary General Electric (Hendersonville, North Carolina, USA) 400-W mercury vapor lamps (photosynthetically active radiation up to 1390 µmol·m–2·s–1). All experiments were repeated at least twice with essentially similar results.

The experiments generally were started when the plants were several weeks old. The two-shoot plants were prepared by decapitating the main shoot just above the cotyledons at the seedling age of about 2 wk. This resulted in the outgrowth of the lateral shoots from the buds in the axils of the cotyledons. Subsequent decapitation and NAA treatments (as described in RESULTS) of one or both of these two shoots were carried out after 1 or 2 wk. Shoots were decapitated with a razor blade about 0.75–1 cm above axillary buds. The NAA was obtained from Sigma Chemical Company (St. Louis, Missouri, USA). Measurements of shoot lengths were made with a ruler.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 LITERATURE CITED
 
In the first experiment (Fig. 1, Table 1), which demonstrates apical control and the lack of repressive effects of exogenous auxin, the two highest lateral buds were released by decapitation above the fourth node. After these buds had grown out for 8 d, the higher and the longer branch (B) was removed and the remaining stump's cut surface was treated with auxin (1% NAA). The effect of the removal of this dominating branch (B) accelerated the elongation of the lower dominated branch (A). Treatment of the remaining stump of the upper branch (B) with NAA had essentially no inhibitory effect on elongation of the latter as observed after several days.



View larger version (13K):
[in this window]
[in a new window]
  		Fig. 1. A demonstration of apical control and the effects of auxin (1% NAA). The higher dominating B branch was removed by decapitation (as shown by the short line across the stem) near the base of the branch and treated with or without 1% NAA in lanolin. The lower branch A is the dominated branch. Data are shown in Table 1

 

View this table:
[in this window]
[in a new window]
  		Table 1. A demonstration of apical control of the elongation of the lower dominated shoot A by the upper dominating shoot B and the lack of repression of A by the application of auxin (1% NAA in lanolin) to the cut stump surface of the removed B shoot in Ipomoea nil (Fig. 1). The elongation (in centimeters, means ± SD) of the lower shoot A 6 d after the beginning of the treatment is shown. N = 11–13

 
The second experiment (Fig. 2, Table 2) was a test on the effects of exogenous auxin on both apical control and apical dominance in two cotyledonary shoot plants with unequally sized shoots (i.e., with one shoot [B] dominating the other [A]). After about 2 wk the dominant long shoot (B) was decapitated and treated with 1% NAA (left figure). Compared to the intact controls (wherein shoot B was left intact), the short shoot (A) of the plants with the decapitated long shoot (B) was released from apical control and greatly accelerated in length (Table 2, top). Treatment of the cut stem surface of the decapitated long shoot (B) with 1% NAA strongly inhibited outgrowth of its lateral bud (B shoot LB) below but had no inhibitory effect on the enhancement of elongation of the short shoot (A). Hence, although apical dominance was restored by exogenous auxin, apical control was not.



View larger version (20K):
[in this window]
[in a new window]
  		Fig. 2. (Left) a demonstration of apical control and apical dominance and the effects of auxin (1% NAA) on each (Table 2 , top). The larger dominating B shoot was decapitated high (as indicated by the short horizontal line across the stem), thus retaining its lateral bud (LB) below and treated with or without 1% NAA in lanolin. (Right) the same experiment with a separate group of plants demonstrating only apical control with the B shoot decapitated very close to its base thus shortening the NAA transport distance to the A shoot and eliminating its LB (Table 2 , bottom)

 

View this table:
[in this window]
[in a new window]
  		Table 2. Top: A demonstration of elongation repression of lateral bud (LB) on the dominating shoot B by apical dominance and of the dominated shoot A by apical control, respectively, and the differential effects of exogenous auxin (1% NAA in lanolin) on each when applied to the decapitated shoot B in two-shoot plants (Fig. 2, left). The elongation (in centimeters, means ± SD) of shoot A and of bud LB on shoot B after 5 d. Bottom: The same experiment was done with a separate group of plants with one modification. The decapitation and auxin treatment were carried out very low on shoot B, thus eliminating the LB (Fig. 2, right). N = 9–10

 
Also included in this second experiment (Fig. 2, right; Table 2, bottom) was a variation in the treatment that involved greatly shortening the NAA transport distance between the long dominating shoot (B) and the smaller dominated shoot (A). This was accomplished by decapitating the long shoot to within 1 or 2 cm of its base adjacent to the short shoot. Hence, the applied NAA to the cut surface of the long shoot was nearly touching the base of the short shoot (A). This alteration also eliminated all lateral buds on the long shoot (B) and thus essentially restricted this to a test of apical control of the short shoot (A). Even with this greatly shortened transport distance, NAA had no effect on elongation of the short shoot and hence, apical control.

In the third experiment (Fig. 3, Table 3), the shoot was gently bent down just above one of the high nodes (fifth, sixth, or seventh), and the inverted terminal bud was tied below to a stake with a string. After 5–7 d the growth of the inverted terminal bud began to slow down and the highest lateral bud (HLB) adjacent to the bend in the shoot began to grow out. After several more days the HLB grew to a length of 3–5 cm (Cline, 1983 ; Cline and Riley, 1984 ). Then the entire shoot was straightened up and the terminal bud was returned to its original upright position, whereupon it resumed its normal vigorous growth exerting apical control over the growing HLB below. After several days the main shoot was decapitated just above the slow growing HLB and treated with 1% NAA. As in the two previous experiments, NAA had no significant effect in restoring apical control. The advantage of this system was that it was similar to the Thimann-Skoog experiment for demonstrating the role of auxin in apical dominance. Inasmuch as there was only one shoot in which auxin transport occurred (i.e., the auxin did not have to move across to another branch as in the two earlier experiments), the pathway of auxin transport was entirely downward (basipetal) except for that extending into the relatively short upward-oriented HLB.



View larger version (24K):
[in this window]
[in a new window]
  		Fig. 3. The effects of auxin (1% NAA) on apical control induced by gravitational manipulation of the main shoot (Table 3 ). Following shoot inversion to induce the outgrowth of the highest lateral bud (HLB) adjacent to the bend in the stem and the subsequent straightening up of the shoot to reestablish control by the shoot apex, the main shoot was decapitated just above the HLB and treated with or without 1% NAA

 

View this table:
[in this window]
[in a new window]
  		Table 3. The effects of auxin (1% NAA in lanolin) on apical control induced by gravitational manipulation of the main shoot (Fig. 3). Following shoot inversion to induce the outgrowth of the highest lateral bud (HLB) adjacent to the bend in the stem and the subsequent straightening up of the shoot to reestablish control by the shoot apex, the main shoot was decapitated just above the HLB and treated with or without 1% NAA. The HLB lengths (in centimeters, means ± SD) are shown under different treatments 5 d after the NAA application. N = 4 or 5

 
The fourth experiment (Fig. 4, Table 4) was a test to determine whether exogenously applied auxin to a cut stem surface could move into an already growing short branch and repress its continued elongation. To do this, single-shoot plants were decapitated above their fourth or fifth nodes without any chemical treatment. After 4 or 5 d, the highest lateral buds (LB) had grown out to some extent. The same shoots were decapitated again a centimeter or two below the first point of decapitation, thus retaining all the growing HLBs. Immediately following this second decapitation, the newly cut stem surfaces were treated with and without 1% NAA. After 2 d it was determined that the NAA had had no repressive effect inasmuch as lateral shoots (LBs) of both groups of plants had increased 7.3 cm in length (Table 4). This result would appear to exclude auxin as a repressor of existing shoot elongation (or apical control) in Ipomoea nil.



View larger version (13K):
[in this window]
[in a new window]
  		Fig. 4. The effect of auxin (1% NAA in lanolin) applied to the cut stem surface of the main shoot 2 d after decapitation and after the lateral bud (LB) had begun to grow out (Table 4 ). The first decapitation was to initiate LB outgrowth and the second, after 2 d, was to provide a fresh stem surface for the NAA treatment

 

View this table:
[in this window]
[in a new window]
  		Table 4. The effect of auxin (1% NAA in lanolin) applied to the cut stem surface of the main shoot on lateral shoot elongation (in centimeters, means ± SD) 2 d after decapitation and after the lateral bud (LB) had begun to grow out (Fig. 4). N = 10

 
To more convincingly demonstrate the ability of auxin (1% NAA) to restore apical dominance in Ipomoea nil under various conditions, several kinds of experiments were carried out. The data in Table 5 and Fig. 5 show that although there is strong repression of outgrowth of the first (and highest) lateral bud by treatment of the cut stem surface with NAA in the standard Thimann-Skoog test, there is no repressive effect on the second lateral bud down. In a repeat similar to Snow's two-shoot experiment with nearly equal-size shoots, it is demonstrated in Table 6 and Fig. 6 that NAA applied to the cut stem surface of one of the shoots will not restore apical dominance in the other decapitated shoot, i.e., the NAA will move down in the first shoot (B) and repress its lateral bud (LB-B) but it won't move up acropetally in the other shoot (A) and repress its axillary bud (LB-A) outgrowth.


View this table:
[in this window]
[in a new window]
  		Table 5. The effect of exogenous auxin (1% NAA in lanolin) applied to the cut stem surface immediately following decapitation of the main shoot on the mean lateral bud outgrowth at the first and second nodes down (Fig. 5). The lengths (in centimeters, means ± SD) were measured 6 d after treatment. N = 9

 


View larger version (14K):
[in this window]
[in a new window]
  		Fig. 5. A treatment to determine the effects of exogenous auxin (1% NAA) on the first and second lateral buds (LB) below the point of decapitation (Table 5 )

 

View this table:
[in this window]
[in a new window]
  		Table 6. The effect of exogenous auxin (1% NAA in lanolin) in restoring apical dominance in decapitated two-shoot plants (Fig. 6). Measurements of lateral bud (LB-A/LB-B) or branch length (in centimeters, means ± SD) of shoots A and B were made 5 d after treatment

 


View larger version (18K):
[in this window]
[in a new window]
  		Fig. 6. The effect of exogenous auxin (1% NAA) in restoring apical dominance in decapitated two-shoot plants (Table 6 ). The approximate positions of decapitation of both shoots are shown with the horizontal lines across the stems. LB-A is the lateral bud or branch on A shoot and LB-B is that on the B shoot

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
LITERATURE CITED
 
The results of all experiments in this study involving auxin applications to decapitated upper shoots of Ipomoea nil demonstrated a clear difference in response between apical control and apical dominance. In nearly all cases of the apical dominance experiments there was a strong repressive effect on axillary bud outgrowth by exogenous auxin (1% NAA) whereas in the apical control experiments auxin treatments to the cut surfaces of decapitated (or removed) upper or dominating shoots had little or no inhibitory effect on elongation of the lower growing shoots. Apical dominance but not apical control was restored by exogenous auxin applications in this herbaceous species.

How widely these results can be generalized to other herbaceous plants is unknown, but it has been established that many other species are highly responsive to exogenous auxin in the Thimann-Skoog apical dominance test (Cline, 1996 ). The acropetal (and often upward) transport of auxin appears to be an obvious obstacle in the acceptance of auxin as a repressor signal in apical control. Furthermore, there was no evidence in our study for the existence of an exogenous auxin-induced secondary inhibitor. Even if auxin only moved down the shoot (from the point of application), where it activated a secondary inhibitor, the auxin-induced secondary inhibitor should have acropetally moved up the shoot and inhibited its growth. But there was no such inhibition in any of the experiments. However, there was no doubt whatsoever that the upper intact dominating shoot did somehow exert a strong inhibitory influence upon the elongation of the lower dominated shoot.

One caveat was observed here. If the irradiance level in greenhouse conditions is relatively high, then the lower and older lateral buds on the shoot of a herbaceous plant like Ipomoea nil may often be larger than the upper and younger buds. Hence, following decapitation of the shoot apex, the larger second or third lateral bud down shoot may, at least temporarily, compete favorably or even outgrow the smaller and higher first lateral bud (below the point of decapitation) and apical control, i.e., in the sense of the higher branch being the dominating shoot, at that point will not exist. The investigator may have to wait until and if the upper branch gains dominance or else determine that the lower shoot (under these conditions) is the dominant or codominant one before initiating the treatment. This situation generally does not arise with Ipomoea nil in growth rooms or growth chambers where the irradiance is reduced and the lower lateral buds are smaller and more repressed. In any event, for an apical control experiment, care must be taken to select those plants wherein the upper shoot is clearly dominating the lower one.

Another possible explanation for the lack of response to auxin in the apical control experiments is the longer distance that the auxin must travel (i.e., between the site of treatment and the presumed site of action at the tip of the dominated shoot) as compared with the apical dominance experiment. Although Thimann (1937) reported no effect of variation in transport distance (over a range of 2–150 mm) in etiolated pea seedlings, Cline, Wessel, and Iwamura (1997) have observed in Ipomoea nil that the effectiveness of auxin in repressing lateral buds appears to decline in buds that are beyond 10 or 12 cm (without intervening nodes) from the point of application. With intervening nodes and branching, the distance may be shorter.

The data in Table 5 clearly show that although the highest lateral bud was strongly inhibited by auxin applied to the cut stem surface above, the second axillary bud was not. It grew out to the same extent as the non-auxin control. This same phenomenon has been observed in poplar shoots (data not shown). These and other data suggest that the presence of nodes, branches, and branch junctions in stem tissue may constitute barriers for transport of exogenously applied auxin. Hence, even in apical dominance experiments involving tissues that are very responsive to exogenous auxin, the transport distance and anatomical barriers can limit responses in Ipomoea. However, in a variation of the first apical control experiment, in which a number of nodes were interspersed between the dominant and dominated branches and hence, the intervening transport distance of the inhibitory influence was greatly increased, the inhibition on the lower branch growth was still significant, as was demonstrated by its accelerated elongation following decapitation of the upper dominant branch (data not shown).

In tall trees, the time for auxin transport over the very long distances involved would appear to be months, as the reported slow polar transport velocities are 1 cm/h (Sundberg and Uglla, 1998 ). It is possible that apically derived auxin moving down a trunk could promote cambial-produced auxin so that through repitition of this process down the tree it would be unnecessary for the same auxin molecule to move the entire length of the trunk (B. Sundberg, Swedish Agricultural University, personal communication).

In some experiments in this study, variations in the experimental procedure were made to shorten this auxin transport distance (usually by reducing the length of the downward basipetal stem portion), but these manipulations appeared to have no effect in facilitating auxin action in apical control as judged by subsequent repressive effects on shoot elongation. Whenever there was a requirement for significant acropetal transport of exogenously applied auxin for either bud or possibly shoot repression, the repression never occurred, presumably because acropetal transport did not occur.

That apical control in herbaceous plants is a widely occurring phenomenon is clearly shown in the first two experiments with Ipomoea nil. A vigorously growing dominant shoot or branch suppresses the growth of a lower branch or shoot tip, as is demonstrated by the growth acceleration that occurs in the lower dominated branch or shoot tip when the upper dominant shoot or branch is decapitated or removed. By what means does the growing higher branch repress the growing lower branch? Does the higher branch send down some repressor signal? Does the vigorously growing higher branch constitute a metabolic sink that monopolizes available nutrients and thereby starves the lower branch? Although Thimann's (1977) interpretation of Snow's (1937) two-shoot experiment with Vicia faba discounts any primary role for control of axillary bud growth by cotyledon nutrient supply, the possibility of nutrients playing a significant role in apical dominance and apical control always looms in the background and cannot be completely excluded.

Because apical control of growing branches is similar to apical dominance of axillary buds in some obvious ways, it becomes necessary when attempting to define their causal control mechanisms to precisely elucidate significant physiological distinctions between the two processes. Sachs (1991) , in an admirable effort to paint a broad picture of major correlative controls in plant development, has visualized quantitative variations in the degree of apical dominance in different species exhibiting a wide spectrum of bud outgrowths, e.g., from moderately long branches to strongly inhibited axillary buds. Accordingly, he states, "auxin replaces all the correlative effects of a shoot apex" (p. 27) and is the signal that inhibits lateral bud growth. Hence, there is the implication that if completely inhibited lateral buds are under strong auxin control, then elongating branches under apical control (a weaker expression of apical dominance) are under a reduced level of auxin control. He observes that "inhibition of bud growth by a dominant shoot is more pronounced than by applied auxin" (p. 26). He also suggests the involvement of other signals.

As mentioned in the introduction, many workers, including Brown, Alpine, and Kormanik (1967) , Leakey and Longman (1986) , Suzuki (1990) , and Wilson (2000) , who have been involved with studies of woody species, have articulated significant distinctions between apical control and apical dominance. There is a difference between a growing shoot and an inhibited axillary bud. One has grown out and the other has not. There are most probably some differences and some similarities involved in the growth control mechanisms of each. The degree of quantitative and qualitative differences remains to be elucidated. As was summarized by Cline (1997) , the effects of treatments with various hormones can differ significantly depending on whether they are given to an inhibited lateral or to a growing shoot. Wickson and Thimann (1958) applied auxin to isolated pea buds after 24 h and found that there was little or no repression of bud outgrowth as there was following immediate application. This result coincides with the effects of our auxin treatments in the fourth experiment in the present study after 4 or 5 d.

Under appropriate circumstances the addition of auxin to a growing shoot can enhance elongation (Sachs and Thimann, 1967 ). The crucial point in apical control is whether or not there has been an alteration in the existing growth rate of a branch, whereas in apical dominance the crucial point is whether or not the lateral bud has begun to grow out. Apical dominance determines how many branches grow out and apical control determines their lengths and is controlled at a later stage of growth.

Shein and Jackson (1971) , as well as Stimart (1983) , have stated that a "disturbing" aspect of the apical dominance literature is that a distinction is not usually made between the initiation of axillary bud growth and subsequent elongation, which appear to be under the control of different hormones, as Sachs and Thimann (1964 , 1967 ) have demonstrated with auxin, cytokinin, and gibberellin. Hence, the physiological evidence favors such a distinction (Cline, 1997 ), which has relevant implications for distinguishing between apical dominance and apical control. Maintaining such distinctions in terminology between these two types of correlative control will be helpful in the physiological studies of these separate but interactive causal mechanisms.

To summarize, our definition of apical control involves three elements: (1) A longer, dominating branch or shoot is repressing the elongation of a shorter dominated branch. (2) The shorter dominated branch, although growing more slowly than the longer, dominating shoot or branch, is nevertheless elongating and is not an inhibited lateral bud. (3) The dominating shoot or branch, being younger, is located higher on the main stem than is the dominated branch, although circumstances might be envisioned where the greater height location of the dominating branch would not be an absolute requirement for correlative inhibition. Hence, apical control, as defined here, is a specialized kind of correlative inhibition where the dominating branch or shoot is located higher than the branch or shoot being repressed, as in first and third experiments. The dominating shoot can be an upper branch as in Fig.1 or the upper main shoot as in Fig. 3. Although, as in the two-shoot experiments in Fig. 2, where both the dominating and dominated branches originated at the same location and height from the main stem, the growing apex of the dominating shoot B was higher than that of the dominated shoot A, suggesting that some repressor signal was being communicated from the higher apex B to the lower apex A.

The results of the present study suggest a significant role for auxin as a repressor signal in apical dominance but no evidence for such a role in apical control in Ipomoea nil. If auxin is not the repressor in apical control, then it must be assumed that there are other such functioning signals. The possible role of competition between branches for nutrients cannot be overlooked.

Apical dominance and apical control refer to correlative phenomenon involving signals operating over long distances to suppress lateral bud outgrowth at a very early stage and to suppress branch growth at a later stage, respectively. Recognizing the greatly increased complexity of temperate woody species with respect to perennial growth, winter dormancy, and high woody content over that of herbaceous plants, it is hoped that that the fundamental apical control responses observed here in Ipomoea may be helpful to some degree in understanding these processes in woody plants. In order to understand whole plant or whole tree growth it is necessary to understand how branches influence and control each others' growth.


   FOOTNOTES
 
1 The authors thank Drs. T. Sachs, B. Wilson, and J. McDonald for their helpful input and Dr. M. Evans for his assistance on the figures. Back

2 Author for reprint requests (cline.5{at}osu.edu ) Back


   LITERATURE CITED
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Brown C. R. Alpine P. Kormanik 1967 Apical dominance and form in woody plants: a reappraisal. American Journal of Botany 54: 153-162[CrossRef][ISI]

Cline M. 1983 Apical dominance in Pharbitis nil: effects induced by inverting the apex of the main shoot. Annals of Botany 52: 217-227[Abstract/Free Full Text]

Cline M. 1994 The role of hormones in apical dominance: new approaches to an old problem in plant development. Physiologia Plantarum 90: 230-237[CrossRef]

Cline M. 1996 Exogenous auxin effects on lateral bud outgrowth in decapitated shoots. Annals of Botany 78: 255-266[Abstract/Free Full Text]

Cline M. 1997 Concepts and terminology of apical dominance. American Journal of Botany 84: 1064-1069[Abstract]

Cline M. 2000 Execution of the auxin replacement apical dominance experiment in temperate woody species. American Journal of Botany 87: 182-190[Abstract/Free Full Text]

Cline M. L. Riley 1984 The presentation time for shoot inversion release of apical dominance in Pharbitis nil. Annals of Botany 53: 897-900[Abstract/Free Full Text]

Cline M. T. Wessel H. Iwamura 1997 Cytokinin/auxin control of apical dominance in Ipomoea nil. Plant and Cell Physiology 38: 659-667[Abstract/Free Full Text]

Cook N. E. Rabe G. Jacobs 1999 Early expression of apical control regulates length and crotch angle of sylleptic shoots in peach and nectarine. HortScience 34: 604-606[Abstract/Free Full Text]

Gunckel J. K. Thimann R. Wetmore 1949 Studies of development in long shoots and short shoots of Ginkgo biloba L. IV Growth habit, shoot expression and the mechanism of its control. American Journal of Botany 36: 309-316[CrossRef][ISI]

Hosokawa Z. L. Shi T. Prasad M. Cline 1990 Apical dominance control in Ipomoea nil: the influence of shoot apex, leaves and stem. Annals of Botany 65: 547-556[Abstract/Free Full Text]

Leakey R. K. Longman 1986 Physiological, environmental and genetic variation in apical dominance as determined by decapitation in Triplochiton scleroxylon. Tree Physiology 1: 193-207

Li C-J. F. Bangerth 1999 Autoinhibition of indoleactic acid transport in the shoots of two-branched pea (Pisum sativum) plants and its relationship to correlative dominance. Physiologia Plantarum 106: 415-420[CrossRef]

Little C. 1969 Apical dominance in long shoots of white pine (Pinus strobus). Canadian Journal of Botany 48: 239-253

Morris D. 1977 Transport of exogenous auxin in two-branched dwarf pea seedlings (Pisum sativum L). Planta 136: 91-96[CrossRef][ISI]

Napoli C. C. Beveridge K. Snowden 1999 Re-evaluating concepts of apical dominance and the control of axillary bud outgrowth. Current Topics in Developmental Biology 44: 127-169[ISI][Medline]

Prasad T. Z. Hosokawa M. Cline 1989 Effects of auxin transport inhibitors and mineral nutrients on apical dominance in Pharbitis nil. Journal of Plant Physiology 135: 472-477[ISI]

Prasad T. X. Li A. Abdel-Rahman Z. Hosokawa N. Cloud C. LaMotte M. Cline 1993 Does auxin play a role in the release of apical dominance by shoot inversion in Ipomoea nil?. Annals of Botany 71: 223-229[Abstract/Free Full Text]

Sachs T. 1966 Senescence of inhibited shoots of peas and apical dominance. Annals of Botany 30: 447-456[Abstract/Free Full Text]

Sachs T. 1991 Pattern formation in plant tissues. Cambridge University Press, New York, New York, USA

Sachs T. K. Thimann 1964 Release of lateral buds from apical dominance. Nature 201: 939-940[CrossRef]

Sachs T. K. Thimann 1967 The role of auxins and cytokinins in the release of buds from dominance. American Journal of Botany 54: 136-144[CrossRef][ISI]

Saks Y. I. Ilan 1984 Hormone-mediated regulative action of the sunflower shoot apex on growth and cation level in the cotyledons—an additional manifestation of apical control. Plant Physiology 74: 408-412[Abstract/Free Full Text]

Shein T. D. Jackson 1971 Hormone intereaction in apical dominance in Phaseolus vulgaris L. Annals of Botany 35: 555-564[Abstract/Free Full Text]

Shimizu-Sato S. H. Mori 2001 Control of outgrowth and dormancy in axillary buds. Plant Physiology 127: 1405-1413[Free Full Text]

Snow R. 1931 Experiments on growth and inhibition. Part II. A new phenomena of inhibition. Proceedings of the Royal Society of London B 108: 305-316

Snow R. 1937 On the nature of correlative inhibition. New Phytologist 36: 283-300[CrossRef]

Stafstrom J. I. Sussex 1992 Expression of a ribosomal protein in axillary buds of pea. Plant Physiology 100: 1494-1502[Abstract/Free Full Text]

Stimart D. 1983 Promotion and inhibition of branching in poinsettia in grafts between self-branching and non-branching cultivars. Journal of the American Society for Horticultural Science 108: 419-422[ISI]

Stirk W. M. Aken J. van Staden 1997 Apical control of growth in a filamentous red alga (Ceramiaceae, Rhodophyta). South African Journal of Botany 63: 267-270[ISI]

Sundberg B. C. Uggla 1998 Origin and dynamics of indoleacetic acid under polar transport in Pinus sylvestris. Physiologia Plantarum 104: 22-29[CrossRef]

Suzuki T. 1990 Apical control of lateral bud development and shoot growth in mulberry (Morus albua). Physiologia Plantarum 80: 350-356[CrossRef]

Thimann K. 1937 On the nature of inhibitions caused by auxin. American Journal of Botany 24: 407-412[CrossRef][ISI]

Thimann K. 1977 Hormone action in the whole life of plants. University of Massachusetts Press, Amherst, Masssachusetts, USA

Thimann K. F. Skoog 1933 Studies on the growth hormone in plants. III. The inhibiting action of growth substances on bud development. Proceedings of the National Academy of Sciences, USA 19: 714-716[Free Full Text]

Thimann K. F. Skoog 1934 On the inhibition of bud development and other functions of growth substances in Vicia faba. Proceedings of the Royal Society of London B 114: 317-339

Timell T. 1986 Compression wood in gymnosperms II. Springer-Verlag, New York, New York, USA

Wareing P. 1970 Growth and its coordination in trees. In L. Luckwill and C. Cuttings [eds.], Physiology of tree crops, 1–21. Academic Press, New York, New York, USA

Wickson M. K. Thimann 1958 The antagonism of auxin and kinetin in apical dominance. Physiologia Plantarum 11: 62-74[CrossRef]

Wilson B. 1990 The development of tree form. HortScience 25: 52-54[Free Full Text]

Wilson B. 2000 Apical control of branch growth and angle in woody plants. American Journal of Botany 87: 601-607[Abstract/Free Full Text]





This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Submit a response
Right arrow Alert me when this article is cited
Right arrow Alert me when eLetters are posted
Right arrow Alert me if a correction is posted
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Cline, M. G.
Right arrow Articles by Sadeski, K.
Right arrow Search for Related Content
PubMed
Right arrow Articles by Cline, M. G.
Right arrow Articles by Sadeski, K.
Agricola
Right arrow Articles by Cline, M. G.
Right arrow Articles by Sadeski, K.

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS