Journal Articles courtesy of:
E. J. Fortanier and H. Jonkers
Department of Horticulture
Wageningen, The Netherlands
Acta Horticulture 56, 1976
Juvenility in Woody Perenials
An evaluation of literature leads to the conclusion that ageing and senescence can be related to ontogenctical and physiological causes. Ontogenctical ageing is genetically programmed, localized in the meristems, not related to exhaustion, and cannot easily be reversed. This implies important consequences for vegetative multiplication and for the characteristics of clones obtained. Physiological ageing is correlatively influenced, caused by an increased disorganization and exhaustion, and is not localized in the meristems. When not advanced, a reversal is possible. Senescence regards more often the physiological ageing, but may he of ontogenctical nature.
Terms related to ageing are used in confusion in every language because they are not clearly defined. This regards, for example, 'ageing', and 'senescing', having a similar or different meaning. It indicates the need for a better distinction and description of the ageing processes, of its different phases, the process of 'rise and shine', covering the juvenile and mature or adult phase, which received more attention than the 'fall', representing the phase of full senescence. The latter negative aspect of ageing drew interest more recently and became a new branch of science: phytogerontology.
This paper describes some of the present views with regard to ageing in the sense of becoming more full grown, as opposed to ageing In the sense of getting more deteriorated. It distinguishes an ontogenctical and a physiological type of ageing. This may have implications and consequences for a discussion on 'Juvenility in Plants', the subject of this symposium.
Ageing in plants has three aspects, a chronological, an ontogenetical and a physiological one. In this order they are or, or less indicated by such opposing terms as: young and old, juvenile and adult, improving and deteriorating. There may be no contradiction if a plant is considered 'young and adult' or 'juvenile and senescent'. Strictly taken all three aspects of ageing start from the formation of the zygote or, more in general, from germination or probably regeneration and terminate with the natural death.
Chronological ageing only refers to the time which has elapsed e.g. since the plant germinated, but does not give any information about the ontogenctical phase or physiological condition reached.
Ontogenetical ageing more specifically refers to the process of passing through different phases of development, from germination to complete senescence. Ontogeny is that part of biology which studies the development of a zygote into an adult individual. It Includes 'embryology', the first part of development, and 'morphology', the subsequent change of shape or metamorphosis. Ontogeny normally represents the positive aspect of ageing, which can he depicted by the rising of the sigmoid growth curve. As a rule ontogenetical ageing is Phenotypically visible and often correlated with, and indicated by, characteristics such as the plant size reached, the number of leaves produced, the phyllotaxis shown, or by the absence or presence of flowers. One distinguishes, for example, juvenile from mature or ,vegetative from generative plants. however, these pairs of notions need not be identical. An adult plant may remain vegetative if it is not induced to flower by required specific conditions. This situation does not mean that ontogenesis came to an end, because the terminal meristem then continues to initiate leaves until it receives the proper stimulus to produce flowers, thus affecting the phenotype of the plant.
Physiological ageing applies primarily to the changes within the plant coherent with the 'coming of age' phase. It represents the negative aspects of ageing such as loss of growth vigour, the increased susceptibility to adverse conditions, or deterioration in general. This process of decline can he depicted by the downward course or last part of the sigmoid growth curve. It is usually indicated by the term 'senescence', and normally precedes the actual process of dying off. Senescence may cover the whole plant or only parts of it, and may therefore begin early during ontogenesis. This indicates that ontogenetical and physiological ageing, while different, should not he regarded as completely independent of one another. Both may affect, for example, juvenility and rejuvenation, and determine the life span of the plant or even the durability of its parts when harvested.
Some characteristics of the ontogenctical ageing
Ontogenctical ageing seems to be located in the terminal meristem (Pierik, 1967) while its degree would be dependent on the activity of the meristem, as indicated by the number of cell divisions. The stage of ontogenetical ageing reached is carried over onto its lateral meristems when these are formed (Robinson and Warcing, 1969). This theory is supported by many older conceptions such as topophysis' and 'cyclophysis' (Seeliger, 1924). Both ideas mean about the same, and refer to the phenomena that a cutting or graft will develop depending on, respectively, its former location on the mother plant, or the stage of development at the time of its separation.
The theory that ontogenctical ageing is located in the meristems also explains the presence of an 'ageing gradient' in each plant. A seedling does not age ontogenctically as a whole but it does from the base to the top and from the inner to the outer parts. In plants there is no continuous replacement of cells, such as occurs in animals. This explains the paradox that the first-initiated, lowest, and chronologically-eldest part of a seedling is most juvenile, while its more recently formed periphery is ontogenctically most mature. Full- grown and old seedlings long retain many characteristics of juvenility at their base or reproduce them when forming adventitious shoots at this site.
Ontogenetical ageing Is accompanied by anatomical, cytological and even physiological changes. These were also observed in form, structure and cell properties of the terminal meristems (Ali and Westwood, 1966), and could be used for determining the termination of the juvenile phase. Not much is known about the hormonal regulation of the phase change. It is supposed that the ratio between growth-promoting and growth-retarding substances and/or the amount of a specific hormone are inductive for flowering only after a specific ontogenctical stage, known as maturity, has been reached.
Consequences of ontogenetical ageing
The local differences in a seedling, regarding ontogenctical ageing, may have decisive consequences for the selection of plant parts for vegetative propagation. It may result in big differences in the offspring of a single plant. This regards, for example, the rooting capacity, growth vigour, willingness to flower and even such phenotypic traits of the new plant as leaf shape, branching, stem colour and the property of keeping or shedding the leaves after senescence. It is generally known that adult cuttings from the top are more difficult to root, grow less vigorously and flower sooner than juvenile cuttings from the base of a seedling. Budding or grafting presents a solution when the capability to root is completely absent. This practice, and the exclusive use of adult plant parts, may then lead to the loss of the existence of juvenile tissue. This could explain why some plants, known from older publications as easily to be propagated, cannot be brought on their own roots nowadays (Hartmann and Kester, 1968). It can be questioned however, why one takes into account the proper choice of plant material for vegetative propagation in some crops but not in others. The system of in vitro culture may present answers to some of these questions. Influencing ontogenetical ageing may be of commercial interest in many cases, such as shortening or extending the juvenile period.
Regulation of ontogenctical ageing
Ontagenetical aging can be accelerated by improving growth conditions, shortening endogenous dormancy and avoiding imposed rest. As a rule this leads to accelerated and prolonged activity of the terminal moristem, which increases apical dominance, reducing the branching and its requirement for assimilates, which in itself again leads to an additional stimulation of growth of the terminal bud. In this way the juvenile period and time to flowering can be shortened to a considerable extent, particularly in perennials (Doorenbos, 1965; Zimmerman, 1972). The approach, however, normally does not change the developmental stage, as indicated by the size, stem length or leaf number of the plant at which it starts flowering.
Flowering at an earlier stage of development was induced in some plants almost exclusively by chemicals, gibberellins in particular, or by grafting onto adult plants. An extreme case is the induction of flowering with gibberellins in 8 to 12 months old Sequoia seedlings, of which the juvenile period normally lasts 20 to 70 years (Pharis and Morf, 1969). With gibberellins, as well as with grafting, contradictory results have been published (Zimmerman, 1972). To further complicate matters, most publications do not indicate the stage of development at which the earlier flowering was obtained and what happens when the chemical treatment is stopped. This makes it difficult to judge whether only the juvenile period, or also the juvenile phase, was shortened. In the latter case, a continuation of flowering without a special treatment, and excluding the possibility of an auto-catalytic formation of a hormone for flowering (Wellonsick, 1966), could indicate that ageing was really shortened ontogenctically. This does not seem very likely.
Because the ability to regenerate new organs diminishes with ontogenetical ageing, its retardation may be desired, e.g. for the production of cuttings able to root. This can he achieved by keeping the growth conditions marginal and by regular pruning of the roots when no cuttings are needed. The possibilities of rejuvenation will be discussed later.
Some characteristics of physiological ageing
Physiological ageing can be defined as 'growing old', indicating the loss of vitality ending with death. Senescence is the word commonly used to indicate this process. Initially it may affect only parts of the plant, but inevitably, the whole plant will succumb. Senescence accompanies ontogenctical ageing and terminates it at last. It affects the whole plant contrary to the more specifically located ontogenctical ageing. Juvenility will not prevent a leaf from ageing physiologically. Senescence of a plant may proceed gradually or may be more sudden, affecting all parts simultaneously. At the same time it may be acropetally or basipetally directed. This brings us to the question whether two types of physiological ageing must be distinguished, i.e. one independent and another dependent on the stage of ontogenetical ageing reached by the plant.
Gradual senescence normally starts at the base of the plant and is acropetally directed. It is commonly accompanied by a mobilization of metabolites from the ageing organs by the active parts of the plant, and is obviously a correlative phenomenon. This is supported by the observation that cotyledons or first leaves will age much later if higher located parts of the plant are removed. Moreover, if these parts are rooted, they can reach a much larger size and greater age than would have been possible if they were left on the plant. This so-called compensatory growth is due to increased cell enlargement and DNA content, but senescence cannot he escaped, whether or not accompanied by the occurrence of endomitosis or endoploidy (Butterfass, 1970).
Gradual senescence can also be observed in very old trees or monocarpic plants kept vegetative. This deterioration or dying back, however, has a clear basipetal direction and is not accompanied by a remobilization of reserves. It is a consequence of starvation or exhaustion of the most distant parts and of a disorganization in general. The internal transport path gradually becomes too long, the balance between dissimilation and assimilation and between root and shoot activity is less favourable, while a decreased supply of water, nutrients and minerals limits a continual growth. The only remedy is an extensive pruning back which at the same time induces growth of ontogenetically younger meristems.
Whatever the direction of physiological ageing may be, it is not controlled by the terminal meristems as is the case in the ontogenetical ageing. This is demonstrated by the fact that an ageing top may resume its normal growth after a separation in time and rooting, or in other cases, grafting on a vital plant. Top shoots of old vegetative sunflowers produced more internodes and resumed rapid growth when grafted onto a younger plant (Warcing and Phillips, 1970).. Here senescence completely lacks all characteristics of a preprogrammed process.
One of the oldest living organisms known is a Pinus aristata Engelm. in California. It has a measured age of 4600 years which illustrates that meristems may have a long lifespan. However, it was discovered that mitosis in very old meristems of a number of plants was not normal. This results in a deviating number of chromosomes and in decreased cell division, an indication that physiological ageing may finally affect the meristems themselves.
Simultaneous senescence. More dramatic than general senescence is the annual occurrence of a simultaneous and total senescence in monocarpic plants, of the over-ground parts in perennial plants, and of a total leaf shedding in deciduous plants. Normally, this sudden senescence is also accompanied by a redistribution of metabolites from the dying plant parts to the surviving organs, such as seeds, bulbs, corms, rhizomes and buds. For this senescence Molisch (1938) already introduced the conception of 'Erschopfungstod.' The idea that exhaustion could be the cause of senescence and death was supported by the observation that a timely removal of the reproductive organs could postpone senescence or prevent death for long. The best known example is Aqave mnericana L., which in its normal habitat flowers in about 8 years and dies subsequently. Death of this monocotyledonous plant is normally induced by the formation of an inflorescence, and therefore is almost ontogenetical by its cause. In climates where no flower induction occurs the plant may become older than a century, but it will not indefinitely escape physiological ageing. A similar type of physiological ageing terminating ontogenesis occurs in maturing crops such as peas. A tip of an aged pea plant does not recover after grafting onto a young plant, while a tip of a young plant grows normally when grafted onto an aged plant (1ockhart and Gottschall, 1961). In monocarpic plants like Agave and pea the sudden and simultaneous senescence seems to have been induced by ontogeny itself. Many investigations demonstrated that exhaustion of metabolites is rather a result than a cause of senescence, beginning normally after most of the fruits have developed. In dioecious plants the males may start senescence long before the females are fruiting.
The periodic leaf shedding of deciduous plants occurs in the juvenile as well as in the adult phase, and is therefore clearly independent of the ontogenetical stage reached. Moreover, it cannot be related to an exhaustion by other plant parts. The sudden and simultaneous occurrence of senescence, however, indicates also in this case a hormonal induction and regulation of physiological ageing.
The examples presented support the supposed differences in the triggering of physiological ageing. The final total plant senescence cannot be regarded as a correlative phenomenon but seems to be governed by the meristems similar to that of ontogenesis itself.
The possibilities of rejuvenation
Rejuvenation is the opposite of ageing and as a consequence of the foregoing discussion, we should distinguish now a physiological and an ontogenetical type of rejuvenation.
Each plant, even a Pinus aristata, cannot escape a final total senescence and death. Prevention of flowering or fruiting does not produce any rejuvenation. In polvcarpic plants it will favour vegetative growth and by that only advance the time of total senescence contrary to the delay of it in monocarpic plants. A severe pruning of the branches or stems is much more effective. It shortens the internal transport system and improves the supply of the periphery with water and nutrients. This can he regarded as a physiological rejuvenation.
Pruning also induces younger buds or tissue to form normal or adventitious shoots, these being more juvenile than those removed. This can he seen as a kind of semi-ontogenctical rejuvenation. Theoretically such a rejuvenation cannot be continued indefinitely, because each pruning activates the meristems present, stimulating their ontogenetical ageing. Better possibilities for the preservation of a plant or tree are nresented by its timely vegetative propagation, as is the case naturally in many perennials. This leads us to the old question of whether clones age or not (Rijhouwer, 1930), including the problem whether all plant cells remain totipotent. In one-cell cultures it appears that the number of non-dividing and dying cells increases with time, notwithstanding a regular dilution of the culture and the presence of sufficient food. Based on extensive experiments with clones of Lemna minor L. (1Vangerminn, 1965) the question regarding the ageing of clones can he answered negatively, provided the proper time and plant parts are chosen for propagation. Yet it cannot he denied that a continuous vegetative propagation sometimes leads to a loss of favourable characteristics (Hartmann and Kester, 1968).
A true ontogenetical rejuvenation would mean that adult meristems could reproduce plants or parts being again completely juvenile. Some examples are nresented by the production of new seedlings after amphimixis or even apomixis, and the spontaneous or artificial regeneration of juvenile plants, either in vitro or in vivo, from all kinds of adult plant parts, such as stems, leaves and flowers (Plerik, 1975). This ontogenetical rejuvenation is much more difficult to explain than the former physiological rejuvenation. It is supposed that an isolation of a single or at least a limited number of totipotent cells from the surrounding tissue is a prerequisite for a totel rejuvenation (Steward, 1967). Comparable results were obtained by grafting juvenile seedlings onto the adult parts of the plant (ivy, sugarbeet, rubber), or by spraying them regularly with gibberellin (Stoutemyer et al., 1961). It should be noted that opposite effects were mentioned earlier, while discussing the probabilities of an accelerated ontopeny.
Summary and conclusion
Juvenility is an important phase in the development of plants. it is depending on, and affected by, a process of ontogenetical as well as physiological ageing and rejuvenation.. Ontogenetical ageing can be considered as genetically programmed, localized in the meristems, accelerated by improved growth conditions and difficult to reverse. It is accompanied or terminated by physiological ageing or senescence. This senescence is correlatively influenced, caused by an increased internal disorganization, and normally not localized in the meristems. If not advanced, its reversal is possible. Only the final and total plant senescence can be considered to be of an ontogenctical nature, located in the meristems, and as such irreversible. These conceptions may imply important consequences for vegetative multiplication, both in vitro and in vivo, and for the characteristics of the clones obtained. It probably supports the necessity of further research on the effects of ontogenetical and physiological ageing of plants in the culturing of their meristems and tissues.
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