Dept. of Agriculture, Technical Bull. No. 1293, pp. 62-65.
Meristems, Growth, and Development in Woody Plants
J. A. Romberger
U.S. Department of Agriculture, Forest Service
Shoot Tip Abortion
Inability to Form Terminal Buds
Many common angiospermous trees and shrubs never form persistent terminal buds. Their shoot tips die and are abscised each season. The uppermost surviving axillary buds then become pseudoterminal buds, and growth proceeds from them the following season. Mohl (1844, 1848, 1860), and others before him (see Lubbock 1899), already knew that shoot tip abortion cannot be ascribed to late spring or early autumn frosts and that it is a natural, nonpathological phenomenon. Lubbock (1899, pp. 9-10) had this to say:
There is a remarkable point about the Lime and some of our other forest trees and shrubs, which Vaucher [Soc. Phys. et Hist. Nat. Genève 1: 296, 1822] seems to have been the first to notice, namely, that the terminal buds die, and that very early .... If a branch be examined a little later, it will be found to be terminated by a scar, left by the true terminal bud, which has dropped away, so that the one which is apparently terminal is really axillary.
The same thing occurs in the Elm, Birch, Hazel-Nut, Lilac, Willow, &c. In these and many other species the bud situated apparently at the end of the branchlets is in reality axillary, as is shown by the presence of a terminal scar, due to the fail of the true terminal bud. I have found that even at the end of May the terminal buds of the Lime have almost all died and fallen away.
But why do the terminal buds wither away? In some cases the bud contains a definite number of leaves, but in the genera above mentioned the number is indefinite—more than can come to maturity; and yet the rudiments, which are constructed to produce true leaves, cannot modify themselves into bud-scales. Thus, in the Ash, Maple, Horse Chestnut, and Oak, which have true terminal buds, there are comparatively few leaves; while in the Elm there are about seven, Hornbeam eight, Lime eight, Willow fifteen, and Lilac fifteen.
In the above species it is generally the uppermost lateral bud or buds which develop, but in some cases, as in Viburnum Opulus (the Guelder Rose), Gymnocladus, &c., these also perish, and as a rule only the lower ones grow, and the upper part of the stem dies back.
|10 A partial list of temperate zone genera follows: Salix, Betula, Carpinus, Corylus, Castanea, Ulmus, Celtis, Platanus, Gleditsia, Gymnocladus, Robinia, Ailanthus, Rhamnus, Tilia, Diospyros, Syringa, and Catalpa. Abscission of shoot apices occurs in some tropical genera also (Koriba 1958).|
Since Lubbock wrote the above, a little progress has been made in understanding shoot tip abortion, but the question of why it happens cannot yet be answered. The unadorned statement, "terminal buds lacking," which occurs in botanical descriptions of many genera10 of trees and shrubs, glosses over a great deal of interesting physiology. It implies lack of control mechanisms able to direct development into scales of primordia initiated by the apical meristem.
Yet the first series of primordia initiated by axillary meristems on the same shoot do develop into bud scales. A second series of primordia initiated by each axillary bud meristem develops into leaves. What is lacking is the ability to revert the developmental pattern back to scale formation after a series of leaves has been produced (p. 45). Finally formation of additional leaves is halted by loss of the entire apex with some of the younger leaves and internodes. Thus apical growth of each shoot is determinate, but growth of the whole shoot system is indeterminate because axillary meristems can produce buds.
Physiology of Apical Abortion
Is it possible that under suitably controlled conditions apical abortion can be prevented in those species which normally undergo it? Wiesner (1889) did some experimental work on the problem, using Rhamnus cathartica, and found that abortion of the apex could be prevented by timely removal of lateral buds. Apical growth then continued if plenty of water was supplied.
Later Mogk (1914) studied apical behavior of Tilia ulmifolia, in which the apex and several of the youngest internodes are abscised in May (Central Europe). Mogk found no evidence to support the then current ideas that apical abscission was due to severe competition for water and nutrients between the apex and expanding leaves and internodes below. His results led him to suggest that apical regions cease growth and abort because a constitutional change has been induced in them which prevents utilization of available nutrients and water.
Klebs (1917) attempted unsuccessfully to discover the basis of the constitutional changes suggested by Mogk. He was, however, able to maintain growth and prevent abscission of the apices of well-fertilized and watered Robinia pseudoacacia seedlings for as long as 10 months by bringing them indoors under continuous artificial light during winter. Klebs concluded that removal of leaves and lateral buds is not necessary to prevent apical abortion when the seedlings are exposed to summer daylight or to continuous artificial light and when water and nutrient supply is optimal.
After development of the photoperiodism concept (p. 84 ff.), later workers demonstrated that apical abortion in Robinia (Wareing 1954; Wareing and Roberts 1956) and Catalpa (Downs and Borthwick 1956a; Downs 1958) can be markedly hastened by short photoperiods and delayed by long photoperiods. Photoperiodism is certainly a valuable experimental tool, but the degree to which it controls apical abortion under natural conditions remains to be determined.
Excision of young lateral buds from shoots may delay apical abortion (Wiesner 1889). Removal of very young leaves may also result in additional leaf development at the apex and delayed abortion, but only if a vigorous shoot is chosen for the experiment (Berthold 1904). Axillary bud removal from developing long shoots of Cercidiphyllum japonicum promotes formation of leaves beyond the normal number, but internodes between them gradually become shorter (Titman and Wetmore 1955).
In vigorous shoots of Syringa vulgaris destruction of the uppermost axillary buds promotes renewed growth and delays abortion of the apex. Weak shoots give no such response (Garrison and Wetmore 1961). Obviously young leaves and axillary buds do have an influence upon growth at the apex, but this is probably more subtle than mere competition for water and nutrients.
Syringa vulgaris shoot tips put into nutrient culture medium grow for a time and expand a few leaves, but their apices ultimately abort just as those on intact plants. Abortion occurs even though water stress is not a factor and competition for nutrients can hardly be severe. The first step in abortion is not tissue necrosis, but cessation of growth. In the final stages cellular disintegration occurs and a cork cambium forms across the axis just above the uppermost pair of lateral buds. The tissue above drys up and eventually falls away (Garrison and Wetmore 1961).
I was able to watch abortion of Tilia americana shoot tips near Beltsville, Md., May 22 to 25, 1962. A considerable amount of young shoot tissue is normally aborted by Tilia, and this is not the result of water stress (see Mogk 1914). Prior to abortion tips turn yellow but do not wilt perceptibly. Tips collected just after abortion may still have a water content to 75 to 80 percent. The aborted part includes several partially elongated internodes and partially expanded leaves with stipules and plump, well-developed axillary buds (fig. 5).
An abscission layer is formed just above the uppermost surviving axillary bud and the shoot tip drops away while still alive and well hydrated. Seedlings of Tilia americana occasionally retain their apices and form persistent terminal buds (Ashby 1962). Tilia should provide ideal material for physiological and biochemical study of apical abortion.
Shoot tip abortion is a phenomenon of little practical significance but one of theoretical interest. How did this peculiar method of closing off a season's growth evolve? Or is it perhaps no more peculiar than formation of a terminal bud? What determines the location of the abscission layer or lower limit of abortion? In the terms of Mogk (1914), what constitutional changes prevent utilization of available water and nutrients? These fascinating questions deserve much more attention than they have received so far.
|FIGURE 5.—Top, Shoot tip of Tilia americana just prior to abortion of the part to the left of A. Abscission will occur at A, already marked by an abrupt transition from pale yellow above to green below. After abortion the uppermost surviving axiliary bud B Will become the pseudoterminal bud. (Enlarged about 2 X.) Bottom, Aborted parts of a T. americana shoot. The stipule below was cut away at C to improve visibility. The part to the right of C includes several small leaves with their stipules and well‑developed axillary buds. Total fresh weight of the aborted parts was about 90 mg.; dry weight was about 20 mg. (Enlarged about 2.3 X.)|