The American Horticultural Magazine, 43(3): 161-167 (July 1964)
Juvenility and Flowering Potential in Woody Plants
V. T. Soutemyer*
*Department of Floricultnre and Ornamental Horticulture, University of California, Los Angeles, California.

Hedera helix, showing leaf changes from seedling to adult stage.

The breeding of woody plants, especially tree fruits and forest trees, is generally slow and expensive. Highly trained, ambitious plant breeders and geneticists frequently avoid this group of plants and tend to turn to the herbaceous crops. Short cuts are urgently needed. Unquestionably some progress has been made in accelerating flowering and fruiting but successes are reported more often with clonal materials than with seedling progenies. The breeding of ornamental trees and shrubs is likewise one of the great undeveloped frontiers of horticulture and more rapid evaluation of progenies would also be helpful here.

Plants commonly progress through a series of morphological changes as they go from the seedling to the mature fruiting stage. Sometimes the differences are so slight and gradual that they are not apparent to the casual observer but in other cases they are striking. Some Australian acacias have pinnate leaves in the seedling stage, but after a few months or years lose them and produce only phyllodes in place of the leaves. On the other hand, in some conifers, the change to mature foliage may require many years, and a substantial part of a century may be required in some New Zealand species. Sometimes two different binomials have been given to the same species by taxonomists who were deceived by the varied expressions of growth.

There are often transitional stages between juvenile and mature plants. Frost (1952) was unable to observe that with nucellar citrus lines which originally exhibit pronounced juvenile characters, more thorniness resulted from taking budwood from a low position on trees with the younger nucellar clones, but not with the older. This observation seems to support the traditional view that the lower part of the tree tends to remain more juvenile in character. Cameron and Soost (1952) stated that a few juvenile characters still were observable in some nucellar lines 22 years old.

The German plant physiologist Goebel (1900) was probably the first to systematize and formulate the concept of distinct growth phases in plants. The German botanist Diels (1906) wrote one of the few books on the subject which, however, was descriptive rather than experimental. Diels was much interested in precocious flowering and emphasized that there was great variability in the expression of this character. He observed early flowering in seed pans of mahogany and noticed other cases in dwarf forms of some plant species. Apparently his great interest in plant polymorphism arose from his studies of Australian plants.

Juvenility and Flowering

Usually there is a definite correlation between the attainment of the juvenile foliage type and readiness to produce flowers and fruit. However, certain conifers, olives, and eucalyptus have been observed to bear fruit on shoots bearing juvenile characters. Citrus seedlings sometimes flower exceedingly early in life andƒ then do not flower again for a number of years. On this basis, a number of European pomologists such as Kemmer (1947) (1950) and Natividade (1943) (1957) do not recognize close relationships between type of vegetative growth and flowering. Observations pertinent to the possible relationship of juvenile foliage types to flowering were made on the olive by Natividade (1943), who represents the type of view presented by Kemmer. He found that the suckers which often develop abundantly on the bases of trunks of olive trees on the root-bearing mammillae exhibited some striking similarities in their foliar characters to seedlings of similar age. The seedling leaves were much more rounded than the leaves of the mature tree which are long and slender. Heavy applications of fertilizer and severe pruning tended to accelerate their production and to augment the period of time during which this form of growth is stabilized. Natividade did not believe that this reversion to seedling types of leaves represented a recapitulation of ancestral forms. He believed that the frequent occurrence of juvenile type shoots on the upper parts of the tree, together with the observance of abundant fruit formation on these reversion shoots in the live variety 'Galega', disproved the classic conceptions of Goebel on the juvenile form. He believed that these idiosyncrasies of growth represented merely changes in the nutritional and hormonal balances within the tree. Another possible reason for the divergence of his concepts from those which were formulated by Goebel was that in his experiments, the relative ease of rooting of cuttings was not related closely to the expression of juvenile growth characteristics.

The subject has not been reviewed comprehensively. Stoutemyer (1937) treated certain aspects of the problem in relation to pomology. Sax (1962) has recently covered the same field. Probably the most comprehensive review available is that of Schaffalitzky de Muckadell (1959) who incorporated much of the work by foresters on the problem. Higazy (1962) has also made a similar review, but with particular emphasis on herbaceous plants.

Schaffalitzky de Muckadell (1959) uses the term ''meristematic aging' to express the gradual transformation from an early growth stage to a later. This may be a desirable term as long as it is hot used in a way which would suggest that the process is entirely irreversible. Recent work in our laboratory has revealed convincing evidence that the changes of growth phase are associated with changes in cell behavior which are relatively stable and which can be carried on through many generations in tissue cultures.

Reversion to Juvenility

The reversion to juvenility or the prolongation of juvenile growth is highly advantageous in propagation. However, once this response is not pertinent to our subject we shah treat it very briefly in outline without reviewing the literature.

Reversion shoots come most readily from the roots or the base of the trunk. Reduced light and low nutrient levels both tend to prolong juvenility in plants. Severe pruning or heading back and reduced light and low nutrient levels are helpful. Grafting on juvenile understocks or treatment with gibberellin sometimes produces reversions. Sprouts from adventitious buds on sphaerblasts seem to be juvenile. These are small woody structures which arise in the bark of some trees from independent meristems. The juvenile stage of growth reappears both in the normal seedlings and also in those citrus seedlings resulting from nucellar embryony and may persist in transitional stages for many years.

The principal treatments which have been observed or claimed to favor reversions or the prolongation of juvenility may be listed as follows:

  1. Grafting on juvenile understocks.
  2. Treatments with gibberellins.
  3. Severe pruning or heading back.
  4. Elevated temperatures.
  5. Reduced light.
  6. Low nutrient level.
  7. X-ray treatments.
  8. Cold treatments.
  9. Growth from basal sprouts.
  10. Growth from adventitious buds on sphaeroblasts.

These treatments are of interest to those who are trying to propagate difficult plants such as rubber, but would defeat the objectives of the breeder and will not be discussed here.

Acceleration of Flowering

Treatments which favor early termination of juvenility are of much greater importance in fruit breeding and we shall list the principal methods which have been used. The critical evaluation of the degree of success of some of these treatments is difficult. The flowering of young plants of mature, well-established clones can often be hastened, but responses with young seedlings have been discouraging in many instances. Seedlings used in some reported experiments had often made considerable progress toward the production of flowers.

The following treatments have been claimed to accelerate flowering in seedlings of woody plants. No attempt will be made here to do more than to list treatments systematically and to give a few examples of each.

Use of extra or prolonged growth periods

The theory has sometimes been advanced that certain number of growth cycles must take place before the mature growth stage can be attained. Potapenko (1939) described an experiment in which seedlings of cherry were subjected to two cycles of growth in one year together with suitable adjustment of photoperiods and provision for chilling during the periods of dormancy between cycles of vegetative growth. The seedlings were started into growth in February, and were grown through the first season without interruption. Dormancy was broken on December 27 and the plants were grown to April 1. After a cold treatment the plants were grown from July until late October under an artificially lengthened photoperiod. Growth was started in the following January and some of the seedlings flowered, but no flowering was observed during that year among the control plants. The value of this method is not well substantiated, and other researchers have obtained contradictory results, notably Smeets (1956) who grew seedlings of cherry in a phytotron, giving 3 or 4 growth cycles in two years. All of the control plants flowered, but only one of the treated seedlings.

Dr. Walter E. Lammerts in California obtained early flowering of camellia seedlings through the use of supplementary lights to provide continuous illumination 24 hours per day. Fertilizers were applied liberally and this procedure resulted in blooming at the end of the first year. Longman and Wareing (1959) speeded flowering of birch seedlings by growing under long photoperiods in a glasshouse. Doorenbos (1955) observed that seedlings of rhododendron and azalea likewise respond to supplemental light. Doubtless the list could be extended.

Transplanting and Root Pruning

According to Passy (1909), the French pear breeder Nomblot secured earlier fruiting by transplanting every two years, without pruning or heading back except for light pinching of lateral branches. Scions can be removed with assurance of good results only after the first flowering of the trees.

Geschwind (1880) recommended pruning the roots of young seedlings, cutting back to one half to produce a finer and better branched root system. He stated that frequent subsequent transplanting into richer and better soil induced earlier blossoming.

Root pruning has been observed by foresters to promote cone production on coniferous trees, but sometimes this treatment needs to be combined with heavy nitrogen feeding. Some strains of Wisteria are notably slow in flowering. They frequently respond to root pruning.

Fertilizer Applications

Kolomiec (1952) stated that seedlings of fruit trees must pass through a succession of stages in order to attain the flowering stage. He believed that a lack of nutrients may delay this development.

Foresters have noticed that excess fertilization with ammonium nitrate or root pruning may promote flowering in pine. Spruce responded best if the two treatments were given together. A reduction in shoot vigor frequently results in lessened formation of female pine cones and an appearance of male cones. In general, a high level of nutrition is needed for the development of female cones and a lower level for the male.

Geotropic responses

Bending stems to a horizontal or descending position frequently aids flower bud formation. A system of training pear tree limbs was once developed by bending branches down and weighting bricks. Espalier training of conifers has been observed to aid seed production.

De Silva and Chandrasekera (1959) ring-banded six inches above the graft union and bent the budshoots and secondary shoots into a horizontal position. This treatment Induced flowering in several Hevea rubber tree clones two years after planting.

The use of a klinostat in which the plants are rotated in a horizontal position usually results in increased flowering.

Mound layering

Kuzmin (1910) claimed to be able to accelerate the flowering of seedlings of grape by mound layering the seedlings when they were three to four years old. In this was fruiting was obtained in three to four years in place of the usual live to eight years or more. These main shoots were not headed back at the time the plants were transferred from the seed flats to the field. This treatment is difficult to evaluate.

Bark inversion, ringing, and notching

The inversion of rings or bark on fruit trees has been observed by horticulturists in a number of countries to cause a dwarfing effect on fruit trees. Apparently the abnormal phloem and xylem conducting tissue formed under such circumstances is responsible for the reduction of growth. The effect is apparently temporary since normally polarized conducting elements form at the vertical seam of the ring and in a few years gain sufficient size to function normally.

Sax (1962) reported that by inverting a ring of bark before early July and fastening with a rubber band to heal, ordinary nursery apple trees two or three ears old formed flowers and fruit the following year. Sax however did not try the technique with seedlings and thought that it would probably be ineffective.

Girdling, ringing, and notching have been used also with some success. An unusual treatment which Sax used has been to tie the young seedling plants in a knot at about crown level. The effects of these treatments while sometimes not permanent were often sufficient to establish initial flowering.

A possible explanation of the many discrepancies in the literature here has been furnished by Murawski (1957) who found that the response was strongly related to the position of the bud on the seedling, those from near the base showing much more juvenile tendency than those near the tip of the seedling. Murawski also stressed the importance of permitting apple seedlings to pass through the juvenile stage before budcling them on a dwarfing stock such as Malling IX.

Grafting or budding in crowns of mature fruiting trees

The experiences of those who have tried this method of hastening fruiting have been highly contradictory. Apparently much depends on the stage attained by the seedling before the scion is removed and inserted. Nutritional conditions on the tree into which the scions are placed Undoubtedly would also be important. This variability of response has been characteristic of results both with dwarfing and standard under-stocks.

The question has been studied by Spinks (1925) who found a variety of treatments, both alone and in various combinations, did not seem to advance the period of first flowering appreciably in apple seedlings. Among the factors included were pruning its two degrees of severity, shaping and light pruning, in contrast with no pruning; spring application of mixed complete mineral fertilizers, ringing of branchies in May, root pruning, topworking into bearing trees and growing in pots. None of the treatments were effective.

Zaharov and Potapenko (1939) were not able to advance the fruiting of apple seedlings by grafting two-year scions into the crowns of bearing trees. However, scions from older seedlings which had attained the fruiting stage came into bearing in the second year.

Sen (1942) observed precocious flowering of mango seedlings between two and three years of age used for March grafting and suggested that this may have been due to the influence of the mature trees. Normally seedlings would not be expected to flower until at least six years old.

Sorensen (1943) stated that by budding of Hevea in the crowns of trees of an age of 4 to 10 years, flowering could be induced in three years in contrast to the six or seven years ordinarily required to flower one year budlings. Similar results have been claimed with coniferous evergreens.

Grafting on related species

Another variation of grafting which has been successful involves grafting seedlings on understocks of an entirely different species. A striking illustration is provided in the experiments of Campbell (1961) who by budding on apomictic seedlings of Malus sikkimensis produced flowering in 15 per cent in three years and 53 per cent in four years. Fruiting was obtained in one‑third of the trees in the fourth year. The normal length of time for bearing in these seedlings was 7 to 14 years and the use of the Malling IX understock only shortened the period one year and frequently introduced virus.

This seems to be a promising technique which could be investigated thorougly although it may cause some problems in delayed incompatibilities. However, these can be ignored if the combination will survive long enough to be evaluated by the breeder.

Grafting on Dwarfing Stocks

The vast pomological literature on this subject is highly confusing and contradictory, with many reports of failure. There has apparently been much variability in the results. A certain minimum period seems to be necessary in order to change from juvenile to adult characteristics. Tydeman (1961) found that the length of the juvenile period varied with seedling clones and with different understocks. Seedling apples on the MaIling IX understock flowered 43 per cent at six years in contrast to only 3 per cent on the controls, Flowering was 38 per cent on understock No. 3431 and 9 per cent on the controls.

This technique does not seem to be as promising as grafting on related species, and the accelerations which have been claimed have usually been small.

Grafting mature scions into seedlings

The Russian fruit breeder, Michurin, claimed to be able to hasten the first flowering of fruit tree seedlings by grafting scions of mature clones on them. We have not seen experimental data presented to support this contention. This is doubtless an outgrowth of his "mentor grafting' theories which are still widely supported by many plant breeders in the Soviet Union.

Climatic factors

Seedling fruit trees have been observed to bear earlier in localities having most favorable climate and growing conditions. Cone formation on certain conifers has been observed to be correlated with sufficiently high summer temperatures.

Chemical growth regulators

The recent use of chemical growth depressants to set flower buds uniformly in azaleas suggests that this type of chemical may eventually be used in the solution of these difficult problems.

The outline above is intended to indicate the present day approaches to the question of flowering in woody plants which has been much neglected as a consequence of the greater emphasis on the biology of flowering in herbaceous annual and biennial plants. One of the few experimenters who has worked with woody plants is Wareing (1959), who has formulated an interesting theory. He believed that the basal regions of the tree tend to remain permanently juvenile. The attainment of the adult flowering stage does not usually occur until the tree has attained a certain age, depending on the species in question, and, in his view, requires either (1) the completion of a minimum number of annual growth cycles, or (2) the attainment of a certain minimum size and morphological complexity. In the juvenile condition the annual growth increment is at first high, but it typically decreases markedly as the mature type of growth appears. Wareing suggested that in some species flowering depends on the attainment of the required threshold size during the juvenile phase and in other species on a certain degree of aging of the shoot system. In plants in which flowering is dependent on aging, the juvenile period will naturally be longer than in those which initiate reproduction in the rising phase. Wareing suggested that the transition from the juvenile to the adult state involves differences in the slate o! the cell cytoplasm. Some recent investigations of Stoutemyer and Britt (1963) suggest that the transition involves detectable changes in the cells, since the characteristic growth rates of juvenile and adult. tissue culture are maintained through many subcultures. Recognized facts regarding carbohydrate nitrogen relationships in the flowering of woody plants lit easily into the framework of Wareings scheme. Robbins (1957) has also postulated a chemical basis for the phenomenon of juvenility.

English ivy we find to be a particularly good test subject for studies on juvenility. It has a flattened vining habit with opposite deeply lobed leaves and abundant anthocyanins and aerial roots in the more juvenile growth stages. With maturity, it has entire pointed leaves on a spiral arrangement and rarely forms aerial roots. Tissues or cells from English ivy are comparatively easy to culture in White's (1943) medium with additions of coconut milk, casein hydrolysate and naphthaIeneaeetic acid.

The significant findings of these studies are that the tissue cultures from vine-type shoots have a considerably higher growth rate than those from the shrubby stems. Those from young seedlings are even more rapid growing. Juvenile tissues will grow at lower temperatures. Also, the juvenile cultures form roots much more freely. These differences have persisted two years with monthly subcultures. We believe that this shows that the differences between juvenile and adult growth are profound and are apparently on a cellular basis. Elucidation of the action of the trigger mechanisms which control this change is urgently needed.