American Journal of Botany

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1064

American Journal of Botany 84(9): 10641069. 1997.

CONCEPTS AND TERMINOLOGY OF APICAL

DOMINANCE1

MORRIS G. CLINE

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

Apical dominance is the control exerted by the shoot apex over lateral bud outgrowth. The concepts and terminology

associated with apical dominance as used by various plant scientists sometimes differ, which may lead to significant mis-

conceptions. Apical dominance and its release may be divided into four developmental stages: (I) lateral bud formation, (II)

imposition of inhibition on lateral bud growth, (III) release of apical dominance following decapitation, and (IV) branch

shoot development. Particular emphasis is given to discriminating between Stage III, which is accompanied by initial bud

outgrowth during the first few hours of release and may be promoted by cytokinin and inhibited by auxin, and Stage IV,

which is accompanied by subsequent bud outgrowth occurring days or weeks after decapitation and which may be promoted

by auxin and gibberellin. The importance of not interpreting data measured in Stage IV on the basis of conditions and

processes occurring in Stage III is discussed as well as the correlation between degree of branching and endogenous auxin

content, branching mutants, the quantification of apical dominance in various species (including Arabidopsis), and apical

control in trees.

Key words: apical control; apical dominance; Arabidopsis; auxin; branching; cytokinin; lateral bud outgrowth; shoot

apex.

Apical dominance may be defined as the control ex-erted by the shoot apex over the outgrowth of the lateralbuds (Cline, 1994). This is a classical example of a de-velopmental correlation where one organ of a plant af-fects another organ (Sachs, 1991). Apical dominance isalso referred to as correlative inhibition (Hillman,1984) or in the dormancy literature as paradormancy,a type of growth control involving a biochemical signalfrom another structure (Lang, 1990).

The terminology and concepts associated with apicaldominance as used by molecular biologists, geneticists,ecologists, foresters, agronomists, botanists, horticultur-

ists, and plant physiologists often vary in meaning. Forinstance, do release of apical dominance, bud initi-ation, sprouting, tillering, regrowth, compen-satory growth, release of meristems, branching,feathering, lateral shoot development, axillary budoutgrowth, activation of dormant buds, and branchinduction all have precisely the same meaning? Thereis generally little difficulty as long as there is understand-ing as to the context with which the terms are used. How-ever, in some cases significant misconceptions may arise.

It is the objective of the present essay to explore someof these misconceptions and their implications and to of-fer some suggestions on the quantification of apical dom-inance that may be helpful. Although the scope here is

general, specific discussions on Arabidopsis branchingand apical control in trees are also included.As an apical shoot meristem of a herbaceous plant de-

velops, axillary buds arise exogenously from superficialcell layers in the axils of leaf primordia (Fahn, 1990).These embryonic lateral buds may have inhibition im-posed upon them shortly after their formation or after abrief period of growth. As Steeves and Sussex (1989)

1 Manuscript received 13 August 1996; revision accepted 24 January1997.

The author thanks Carl Leopold, Carolyn Napoli, and Joel Strafstromfor their critical and very helpful comments on the manuscript.

describe, . . .commonly at this time [after bud forma-tion] the dominance of the main apex is expressed in theinhibition of further development of the lateral apices andthey remain as axillary buds, often for long periods andsometimes permanently unless the main apex is re-moved. Although the elongation of the buds may beessentially inhibited, they remain metabolically active(Stafstrom, 1995). As Hillman (1984) points out, Insome species, inhibited or quiescent buds may be fairlyrudimentary whereas in others the buds may be wellformed. . . . If the shoot apex is subsequently decapitat-ed (also sometimes referred to by such terms as apexremoval or excision, clipping, topping, defolia-tion, pruning, trimming, tipping, shearing,heading, herbivory, browsing, meristem de-struction, and pinching), apical dominance is re-leased and one or more of these lower axillary buds be-gins to grow out.

Within a few hours after apex removal, measurable in-creases in the length of the emerging lateral bud can bedetected in some species. In other species the lag periodmay be longer depending upon the degree of inhibitionand the stage of the cell cycle at the time of inhibition(Tamas, 1987). In the days and weeks following decapi-tation, subsequent elongation and development of the lat-eral bud into a branch shoot occur.

These foregoing developmental steps, which will varywith species and will apply more to dicotelydons than tomonocotyledons, may be conveniently divided into fourstages (Fig. 1): lateral bud formation (Stage I), impositionof inhibition (apical dominance) (Stage II), initiation oflateral bud outgrowth following decapitation (Stage III),and subsequent elongation and development of the lateralbud into a branch (Stage IV). Even though there is someoverlap between the four stages, they each involve somedifferent processes and are affected differently by planthormones. Hence, each stage should be considered moreor less separately. The degree of inhibition imposed in


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Fig. 1. Developmental stages of apical dominance before and after release by decapitation of the shoot apex.

Stage II may vary. If it is negligible as with Arabidopsisor greenhouse-grown Coleus (Cline, 1996), then apicaldominance is essentially nonexistent and the lateral budcontinues to grow out from the time of its formation intoStage IV without the necessity of release via decapitation.This is similar to sylleptic growth, which occurs in manytropical woody species and in a few temperate trees (Hal-le, Oldeman, and Tomlinson, 1978; Wheat, 1980) and insome young fruit trees (Barlow, 1970; Tromp, 1996)where there is no rest or dormancy period between budformation and outgrowth.

If the imposition of inhibition is partial as in bean orpetunia, then the apical dominance could be termed asintermediate with a certain level of lateral bud out-growth occurring even without decapitation. If the im-position of inhibition is complete as with Helianthus,Tradescantia, or indoor-grown Ipomoea, then apical

dominance is strong and no release occurs without de-capitation or some drastic restriction of apical shootgrowth. Sachs (1991) describes this as the most extremeform of apical dominance and that the norm involvessome lateral outgrowth even in the intact plant. Speakingmore generally he states: Many physiological studiesstress an all-or-none approach, but this is a result of acareful choice of experimental systems which is dictatedby good reasons of experimental design, not an expres-sion of the common reality of plant development. It isprobably true that among herbaceous species there is awide spectrum of degree of inhibition imposed by apicaldominance and the example that is being portrayed here(Fig. 1) in the four stages is one with relatively strongapical dominance.

STAGES OF BRANCH INITIATION AND BRANCHDEVELOPMENT

Considerable confusion in the literature could be avert-ed if the uniqueness of these four stages could be rec-ognized and some terminology agreed upon. This is par-ticularly true with respect to discriminating between thethird and fourth stages, the initial release of apical dom-inance (Stage III), which occurs in the first few minutesor hours after decapitation and the subsequent or contin-ued elongation of the lateral bud (Stage IV), which occurs

during the following days or weeks after decapitation andresults in the development of a branch shoot. It should

also be emphasized that these developmental states areunder appropriate conditions, reversible (i.e., III to II andIV to II) (J. Stafstrom, personal communication, Department of Biological Sciences, Northern Illinois University).

The release of apical dominance (Stage III) may bepromoted by direct application of cytokinin to the laterabud (Pillay and Railton, 1983) and is often repressed byauxin treatment of the decapitated stump just above thelateral bud (Thimann and Skoog, 1934). In contrast, soonafter apical dominance has been released and lateral budelongation is underway (Stage IV), this developing laterashoot or branch may begin to produce its own auxinwhich may enhance elongation (Thimann and Skoog1934) as may gibberellic acid at this time (Prochazka and

Jacobs, 1984), although Isbell and Morgan (1982) havereported gibberellin repression of tiller growth in sorghum.

Any treatment given to a plant 24 h after apex remova(Stage IV) will have a much different effect on laterabud outgrowth than if it is given immediately followingdecapitation (Stage III). Wickson and Thimann (1958found only a small repression of outgrowth of isolatedpea buds when auxin was added after a 24-h delay. Several workers (Shein and Jackson, 1971; Stimart, 1983)have pointed out a disturbing aspect of the apical domi-nance literature is that a distinction is usually not madebetween the initiation of axillary bud growth and the sub-sequent axillary shoot elongation, which may be under

the control of different hormone factors as demonstratedby Sachs and Thimann (1967).

With respect to hormone effects, the differences instages may be tentatively defined as follows: I (Cytokininpromoted), II (Auxin repressed), III (Cytokinin released)and IV (Auxin and gibberellin promoted).

When considering the mechanism of apical dominancethe physiologist is particularly interested in the processesinvolved in the imposition and release of apical dominance (Stages II and III). A common mistake is to attempto interpret data measured several days or weeks aftedecapitation (during Stage IV when branch development


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is well under way) on the bases of physiological pro-cesses occurring within the first few hours (during StageIII at apical dominance release when the lateral bud firstbegins to grow out). Branch development involves muchmore than apical dominance release and is affected dif-ferently by hormones as mentioned above. What happensin Stage IV is important and valuable to know, but it

should not be confused with what happens in Stage IIIduring apical dominance release.

The perspective taken in this essay is physiological.There certainly are other valid and useful perspectives,e.g., genetic, ecological, etc. Whereas the physiologist fo-cuses directly on the processes (i.e., the imposition/re-lease of inhibition in stages II and III), the developmentalgeneticist may begin by defining the branching gene inStage IV and then work back toward the earlier stages inorder to understand the mechanisms involved (e.g., Na-polis work on petunia, 1996).

BRANCHING AND AUXIN CONTENT

Workers will often use the relative amount of branch-

ing (Stage IV) not only as an indicator of the degree ofapical dominance release but also as a suggestive indi-cator of endogenous auxin content. There is nothingwrong with using branching as an indicator of thestrength of apical dominance as long as it is realized inthe case of branching released by decapitation that thehormonal and other conditions necessary for this releaseare present only during Stage III. Even though low auxincontent in a shoot is correlated with the release of apicaldominance in Stage III and the release of apical domi-nance is a prerequisite for branching, it does not followthat the presence of heavy branching in Stage IV is nec-essarily accompanied by low auxin content. In fact, asthe developing branches produce their own auxin (Thi-mann and Skoog, 1934), the auxin content in Stage IV

may well approach normal levels. That transgenic iaaLtobacco plants deficient in auxin exhibit reduced apicaldominance (Romano, Cooper, and Klee, 1991) probablycan be attributed to the low auxin content at the veryearly stages of bud formation.

The same misconception can occur with the employ-ment of nondecapitated branching mutants (includingtheir use in grafting experiments) for the same reasons asnoted above. Beveridge, Ross, and Murfet (1994) foundthat branching pea mutants had consistently higher en-dogenous free IAA levels than the nonbranching wildtypes. Heavily branching plants should not necessarily beexpected to reflect low endogenous auxin levels. Also,the relative concentration of cytokinins and other plant

hormones as well as the sensitivity of tissues to themcannot be ignored.

QUANTIFICATION OF APICAL DOMINANCE ANDITS RELEASE

In many journal papers (particularly those in molecularbiology) that in some way involve apical dominance re-search, no actual quantitative data on lateral bud out-growth are given. A photograph showing branched andunbranched plants side by side may be included or, moreoften, the degree of dominance or branching under vari-ous conditions are verbally described with such terms as

increased branching, lateral growth, lateral shootformation, bushy, shooty phenotype, reduced ordecreased apical dominance, nonbranching, un-branched growth habit, strong apical dominance, orrestored apical dominance.

Such qualitative visual or verbal evidence may be suf-ficient for many purposes. But in some cases, more quan-

titative and definitive evidence may be required. Whencomparing two plants, what does it mean to say that oneplant has more branching than another? It is probablymeant that one plant has more branches than the other.As experience in Christmas tree selection can attest, out-ward appearance of bushiness can be deceiving. A shortplant with the same number of branches as a tall plantwill appear bushy because of shorter internodes. A plantwith long branches, particularly if they are floppy, mayappear bushier than a plant with the same number ofshorter branches. Secondary and inflorescence branchingwill further complicate the analysis. One plant could havemore branches than another plant if the one plant hadmore nodes, assuming all buds at all nodes on both plantsgrew out. Or, one plant could have more branches if a

greater percentage of its buds had sprouted.Probably the most common way of detecting apical

dominance release is to measure the outgrowth (i.e., budlength or fresh mass) of lateral shoots following decapi-tation or other restrictive treatments of the shoot apex. Inthe case of many herbaceous plants, measurable elonga-tion of the lateral bud begins within 310 h followingdecapitation. The determination of whether or not apicaldominance release at the morphological level has oc-curred depends upon whether or not the lateral bud be-gins to grow out. If the lateral bud has not begun to growout, then it would be presumed that the release of apicaldominance had not occurred. It is understood, of course,that earlier molecular and mitotic events associated with

the release must occur before bud elongation can begin.Since studies on the mechanisms of apical dominancerelease are aimed at understanding these underlying cel-lular, biochemical, and molecular events, it is critical thatthe appropriate determinations and measurements ofthese processes be made both before decapitation in StageII and within minutes and hours after decapitation duringStage III. Continuous measurements of these processesand bud growth can be carried out during the followingdays (Stage IV), but it must be recognized that these datamay not have strict correlation with the mechanisms ofapical dominance release.

EVALUATING APICAL DOMINANCE INARABIDOPSIS

Arabidopsis is a difficult plant for apical dominanceanalysis for two reasons: Firstly, its shoot is an inflores-cence with extremely weak apical dominance (i.e., veryearly branching in the intact bolting shoot). Secondly,there are two types of branches: (1) the inflorescence lat-eral branches, which begin to grow out at the same timeas the main shoot bolts from a rosette base and (2) sec-ondary or axillary inflorescences, which emerge shortlyafter the bolting of the main shoot. Can the release ofapical dominance even be detected following decapitationof the main shoot? The answer to this question is yes, if


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the decapitation is carried out immediately after boltingbegins. There are, of course, quite a range of branchingtypes among the various mutants and lines of Arabidop-sis. The vast genetic data available on Arabidopsis cer-tainly constitute a major advantage for the use of thissystem in branching studies. Mutants with relativelystrong apical dominance include the strain 2100 (Torii

and Komeda, 1993) and the CS 1072 Chi-O (Ohio StateUniversity Arabidopsis Biological Resource Center),whereas those with extremely weak apical dominance in-clude the auxin resistant axr112 (Lincoln, Britton, andEstelle, 1990), the trp11 (Last and Fink, 1988), and theamp1 (Chaudhury et al. 1993).

Branching from the main shoot is not much affectedby decapitation in strain CS 1072 Chi-O (Cline, 1996)because of the extremely early lateral bud outgrowth inthe intact plant. However, the lateral buds below the pointof decapitation grow out longer than those of the controls.Nevertheless, the effect of decapitation of the main shooton hastening the bolting of and increasing the number ofbolting secondary inflorescences is significant and can bedetected in this line. These results probably have general

application to many other lines of Arabidopsis. However,Lincoln, Britton, and Estelle (1990) reported little differ-ence in the total number of inflorescences between thebushy auxin-resistant ax1 mutant and the wild type, al-though there is an increase in the number of lateral shootsin the former.

In most plant species apical dominance release or lat-eral bud outgrowth are usually defined by periodic mea-surements of bud length. In the case of Arabidopsis, suchmeasurements could become cumbersome because of thelarge number of secondary inflorescences that could beencountered. Romano, Cooper, and Klee (1993) used to-tal fresh mass of secondary inflorescences which may bea viable alternative, although it does not distinguish be-

tween inflorescence number and branch length.Although Romano, Cooper, and Klee (1993) did reportinhibition of branching in transgenic iaaM auxin-over-producing plants, Cline (1996) was not able to restoreapical dominance in Arabidopsis by exogenous auxin inlanolin treatment via the classical Thimann-Skoog exper-iment or by aqueous spray. There is concern about thegeneral health of such high auxin-level transgenic plants,which exhibit severe leaf epinasty. Likewise, C. Lincoln(personal communication, Biology Department, IndianaUniversity) was unable to restore apical dominance viaexogenous auxin treatments in Arabidopsis.

For future apical dominance studies with Arabidopsis,the availability of mutants or lines with strong apicaldominance (e.g., NAB 1, Bohmert and Benning, 1996)

would be helpful.

CRITERIA FOR APICAL DOMINANCE ANALYSIS

The ideal plant for analyzing apical dominance releasewith respect to carrying out measurements of lateral budelongation is one with a rapidly growing shoot, moder-ately strong apical dominance (i.e., with inhibited lateralbuds that will respond immediately to decapitation), lat-eral buds that are widely separated by large internodesso as to be easily observed and measured, and a shoot inwhich only the highest lateral bud will grow out follow-

ing decapitation (providing for more uniformity in treat-ments and for a shorter transport distance for chemicalsapplied to the decapitated stump).

Pisum sativum probably has been the most widely usedspecies in apical dominance studies (Wickson and Thi-mann, 1958; Beveridge, Ross, and Murfet, 1994; Stafstrom 1995). These plants are rapidly growing and offer

many advantages. Japanese Morning Glory (Ipomoea nil)is also an excellent system (Cline, 1996). The shoot elon-gates at the rate of 10 cm/d in constant light. Thelateral buds in a 20- to 25-d-old plant average 23 mmin length at the first through the fifth nodes (countingfrom the base). Following decapitation just above thefourth or fifth node, the beginning of elongation can bedetected within 58 h (Yang and Cline, unpublisheddata). The lateral bud at the fourth node (which is similarto that of the fifth node) will have increased in length by1, 5, 17, and 329 mm after the lst, 2nd, 3rd and 7th drespectively (Cline and Riley, 1984). Plants with weakapical dominance, like Coleus, are difficult to study be-cause buds on the intact plant are only slightly inhibitedand, hence, are continually growing out. Decapitation

only slightly hastens bud outgrowth and exogenous auxinadded to the shoot stump of greenhouse-grown Coleusplants has no repressive effect (Jacobs et al., 1959; Cline1996).

An ideal branching mutant would be one that is exactlythe same as the wild type in height, node number, andother characteristics, except that all the lateral buds ointact mutant would grow out, whereas all the lateral budsof the intact wild type would remain inhibited and couldonly be released by decapitation or by some other definitive treatment. If the hormone content or some type ofmolecular/cellular activity is to be compared between thebranching mutant and the wild type plants, it must beremembered that in most situations the branching mutan

will be similar in many respects to the Stage IV plantswhich are far beyond the apical dominance release stage(III).

APICAL DOMINANCE VS. APICAL CONTROL

Although there is some disagreement in distinguishingbetween the meaning of the terms apical dominanceand apical control (Martin, 1987; Loreti and Pisani1990; Wilson, 1990), the former is usually used in a nar-row sense with respect to herbaceous plants to specifycontrol (or correlative influence) by the shoot apex overaxillary bud outgrowth and in a broader sense also toinclude control over orientation of lateral branches andleaves as well as over the growth of branches, rhizomes

stolons, and tubers and, finally, correlative influence overleaf abscission (Hillman, 1984).

Brown, McAlpine, and Kormanik (1967) introducedthe use of the term apical control for woody plantbecause of the complex branching associated with peri-odic sprouting of buds from year to year. Wareing (1970)has stated, . . .the classical theory of apical dominancedoes not seem applicable to shoot systems of woodyplants beyond the first year. Brown used apical con-trol to describe the physiological conditions that giverise to the overall shape and form of the tree crown viavarious branching patterns. The excurrent conifer (e.g.


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pine) has a single dominant central leader shoot andstrong apical control, giving an attenuated-shaped crown.The individual shoots have weak apical dominance andthe lateral buds of the current year grow out to varyingdegrees during the first season. If the growing point issomehow destroyed, then one of the remaining upperbranches, in a Stage IV type response, replaces it by

bending more vertically via processes in the reactionwood and by elongating. Ethylene, gibberellins, and aux-in (Blake, Pharis, and Reid, 1980) may play a role here.

In the decurrent hardwoods (e.g., oak) with no domi-nant leader shoot and with weak apical control (exceptwhen very young), the lateral shoots outgrow the weakleader shoot to give a crown with a round shape. Theindividual shoots presumably have strong apical domi-nance and the lateral buds of the current season do notgrow out until the following spring. Hence, when usedwith respect to trees, apical dominance is thought to referto the control of lateral bud outgrowth by the apex in anindividual branch during the current seasons growth (as-sociated with the Stage III response), whereas apical con-trol refers to the control over branch elongation and ori-

entation (Stage IV events) and is concerned with theinfluence of the main growing point on all branches of aperennial plant (Martin, 1987) or as Bollmark et al.(1995) describe it, the influence of the top of the treeon the branches lower down. . .. However, as Davidsonand Remphrey (1990) have pointed out, The architec-ture of tree crowns may be more complex than the ex-currentdecurrent dichotomy and its relationship to apicalcontrol.

CONCLUSION

In their historical evaluation of adventitious rooting re-search, Haissig and Davis (1994) point out that . . .thereare no rewards, and often criticisms for those who at-tempt to develop terminologies. In the present essaythere has been no presentation of new terms. The per-spective has been physiological and the attempt has beento redefine some of the old terms that relate to apicaldominance such as apical dominance release andbranching along with methods of quantification and toelucidate their usage in a way that, hopefully, will helpgenerate discussion for the future and to avoid miscon-ceptions.

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