Storage and recall of environmental signals in a plant: modelling by use of a differential (continuous) formulation

The breaking of the symmetry of bud growth in Bidens seedlings involves a sort of plant 'memory'. An asymmetrical stimulus (e.g., the pricking of one of the seedling cotyledons) stores a 'symmetry-breaking' signal within the plants (function STO). Depending on other stimuli received by the seedlings, the stored signal may remain silent or be recalled (RCL function) and take effect in the seedling morphogenesis (asymmetry of the growth of the cotyledonary buds, with a statistical advantage to the bud at the axil of the non-stimulated cotyledon). We show that this memory mechanism can be interpreted by a model taking into account a genetic control exerted on a non-linear enzymatic system that is able to choose trajectories going to different attractors, depending on the stimulation intensity.     

Control of a symmetry-breaking process in the course of the morphogenesis of plantlets of Bidens pilosa L.

A mechanism involving transport, storage and retrieval of a symmetry-breaking message controls the relative growth rate of the cotyledonary buds of plantlets of Bidens pilosa L. The asymmetry was induced by administering a few needle pricks to one cotyledon of each plant. The storage of the symmetry-breaking message was independent of the number of pricks (all or nothing process) and irreversible. However, various treatments could render the plants either able to retrieve the stored symmetry-breaking message (in which case, the bud opposite to the pricked cotyledon began to elongate statistically sooner than the one associated with the stimulated cotyledon) or not (both buds then had an equal chance to be the first to start to grow). The retrieval process was also associated with a temporal oscillation. At the level of the whole plants, bud growth was observed only after the removal of apical dominance, and its degree of asymmetry was expressed by use of a parameter g ranging from zero (symmetrical case) to ± 1 (full asymmetry in favor of one of the cotyledonary buds). The highest g-values observed in the present contribution were of the order of 0.5. At the cellular level, the pricking of one cotyledon caused a number of cells, which were within the meristem of the bud associated with the pricked cotyledon and were in cell-cycle phases S or G2, to undergo cellular division and then be blocked in phase G1, whereas the cells of the opposite bud were practically unchanged.We thank Drs. Jean Guern (Laboratoire Hormones végétales, Gif-sur-Yvette, France) Grégoire Nicolis (Service de Chimie Physique II, Bruxelles, Belgique) and Erasmo Marrè (Dipartimento di Biologia, Università di Milano, Milano, Italy) for stimulating discussions, and Mrs. Chantal Eraud, Monique Loiseau and Monique d'Alleizette for their technical assistance.     

Transmission of a traumatic signal via a wave of electric depolarization, and induction of correlations between the cotyledonary buds in Bidens pilosus

Pricking one cotyledon of decapitated plantlets of Bidens pilosus L. induces, i) the induction of a wave of electric depolarization progressing towards the bud at the axil of this cotyledon, and ii) the inhibition of the growth of this bud. The electrophysiologic and morphogenetic responses are dependent on the number of pricks and on the location of these pricks on the cotyledon midribs. When a prick is delivered on the hypocotyl prior to those on the cotyledons, then it prevents the effect of the latter pricks. When it is delivered after those on the cotyledons, it does not change the effects of cotyledon pricking. Our experiments suggest that there is a causal relationship between the electrophysiological and morphogenetic responses.     

The role of endogenous cytokinins in correlation between cotyledon and its axillary bud and in hypocotyl regeneration of flax

When flax seedlings are decapitated above cotyledons and three days later one of the two cotyledons is removed then the remaining cotyledon stimulates in four to five days growth of its axillary bud. It has been found that content of endogenous cytokinins was higher in the stimulated bud as compared with the other one already 12 h after the cotyledon removal. Flax seedlings decapitated under cotyledons regenerate adventitious buds on thy hypocotyl stump during 5–6 days. The endogenous fytohormonal preparation of this regeneration was investigated in the 20 mm apical part of the hypocotyl stump. Decrease in auxin and increase in gibberellins was already found during the first day after decapitation while the level of cytokinins increased as late as three days after the apex removal.     

Hierarchy establishment among potentially similar buds

A plant has a great excess of buds each with the potential of developing an entire shoot system. The general question tackled was to what extent shoot size and time of bud development are important for bud hierarchy. Pea seedlings with two shoots, which were either equal or unequal in size, were obtained by the early removal of the seminal shoot. When these two shoots were also removed, one of the two cotyledon buds next to the bases of the shoots developed into the new shoot system. The determination of which of the buds became dominant was studied as a function of the relative sizes of the two primary cotyledonary shoots, of differences in the timing of the removal of these shoots and of the size of the buds. The bud that became dominant was not necessarily the larger one, nor did it always emerge from the axil of the larger shoot. Instead, it was usually the bud that was inhibited for a shorter period by the shoot next to it. It is suggested that the fate of a bud is predominantly determined by developmental parameters, for example lime of release, which are correlated with its developmental status and not necessarily with its physical size or with the past development of its shoot.     

Memory Processes in the Response of Plants to Environmental Signals

Plants are sensitive to stimuli from the environment (e.g., wind, rain, contact, pricking, wounding). They usually respond to such stimuli by metabolic or morphogenetic changes. Sometimes the information corresponding to a stimulus may be “stored” in the plant where it remains inactive until a second stimulus “recalls” this information and finally allows it to take effect. Two experimental systems have proved especially useful in unravelling the main features of these memory-like processes.In the system based on Bidens seedlings, an asymmetrical treatment (e.g., pricking, or gently rubbing one of the seedling cotyledons) causes the cotyledonary buds to grow asymmetrically after release of apical dominance by decapitation of the seedlings. This information may be stored within the seedlings, without taking effect, for at least two weeks; then the information may be recalled by subjecting the seedlings to a second, appropriate, treatment that permits transduction of the signal into the final response (differential growth of the buds). Whilst storage is an irreversible, all-or-nothing process, recall is sensitive to a number of factors, including the intensity of these factors, and can readily be enabled or disabled. In consequence, it is possible to recall the stored message several times successively.In the system based on flax seedlings, stimulation such as manipulation stimulus, drought, wind, cold shock and radiation from a GSM telephone or from a 105 GHz Gunn oscillator, has no apparent effect. If, however, the seedlings are subjected at the same time to transient calcium depletion, numerous epidermal meristems form in their hypocotyls. When the calcium depletion treatment is applied a few days after the mechanical treatment, the time taken for the meristems to appear is increased by a number of days exactly equal to that between the application of the mechanical treatment and the beginning of the calcium depletion treatment. This means that a meristem-production information corresponding to the stimulation treatment has been stored in the plants, without any apparent effect, until the calcium depletion treatment recalls this information to allow it to take effect. Gel electrophoresis has shown that a few protein spots are changed (pI shift, appearance or disappearance of a spot) as a consequence of the application of the treatments that store or recall a meristem-production signal in flax seedlings. A SIMS investigation has revealed that the pI shift of one of these spots is probably due to protein phosphorylation. Modifications of the proteome have also been observed in Arabidopsis seedlings subjected to stimuli such as cold shock or radiation from a GSM telephone.Key Words: memory, environmental signals, meristems, mobile telephone, bud growth, proteome, plants     

Long-distance transport, storage and recall of morphogenetic information in plants. The existence of a sort of primitive plant 'memory'

An asymmetrical treatment of Bidens seedlings (pricking one of the seedling cotyledons) causes the cotyledonary buds to grow asymmetrically after release of apical dominance by decapitation of the seedlings. The symmetry-breaking signal propagates within the seedlings at a rate of at least a fraction of a millimetre per second. This information may be 'stored' (STO function) within the seedlings, without taking effect, for at least 2 weeks; then the information may be 'recalled' (RCL function), thus permitting transduction of the signal into the final response (differential growth of the buds), as a consequence of subjecting the seedlings to various symmetrical or asymmetrical treatments. A similar behaviour was observed with stimuli other than pricking (including non-traumatic stimuli), with plants other than Bidens (flax, tomato), and with responses other than cotyledonary-bud growth (hypocotyl elongation, induction of meristems, thigmomorphogenesis). There are indications that storage may involve the activation of elements implicated in cell cycle control, and that the last steps of the final response involve genes such as tch1 and hsp70. The adaptive advantage for plants in possessing STO/RCL functions is discussed. Manipulating the STO/RCL functions may have interesting practical applications, e.g. in the resistance of plants to natural stresses. The existence of the STO/RCL functions in plants constitutes an elementary form of 'memory' which may provide an experimental system simpler than the animal brain to test the validity of the theoretical models of interpretation of important features such as memory storage and evocation.     

Hormones and young leaves control development of cotyledonary buds in tomato seedlings

Hormonal and plant factors regulating the development of the inhibited cotyledonary buds of Lycopersicon esculentum Mill. cv. `Fireball' seedlings were studied. Excision of the immature plumular leaves of 5- to 20- millimeter length significantly stimulated bud development after 2 to 4 days, but excision of leaves exceeding 20-millimeter length was without effect. Apical application of 20 microliters of 5 millimolar abscisic acid significantly promoted development of the cotyledonary buds after 6 days. A subapical ring of 0.1 millimolar concentration of 2,3,5-triiodobenzoic acid (TIBA) in lanolin significantly promoted cotyledonary bud development after 11 days. Twenty microliters of 0.1 millimolar 6-benzylaminopurine (BAP) applied directly to the cotyledonary bud loci significantly promoted bud development, but 1 micromolar gibberellin A_4/7 was ineffective. Application of 0.1 millimolar BAP in lanolin to the petiole or hypocotyl was ineffective. However, application of 0.1 millimolar TIBA as a ring around the petioles of the cotyledons or 1-centimeter on the hypocotyl below the cotyledons significantly promoted cotyledonary bud development.     

The release of the cotyledonary shoot ofpisum sativum from inhibition in relation to changes in the levels of endogenous auxins,cytokinins, and gibberellins

Both axillary buds belonging to the cotyledons (cotyledonary buds) start to grow on decapitated pea seedlings, but one of them (the dominant shoot) prevails in growth over the other (the inhibited shoot). If the dominant' cotyledonary shoot is removed, the inhibited shoot is released from inhibition and starts to grow. This release from inhibition of the inhibited cotyledonary shoot is accompanied within two hours from the removal of the dominant cotyledonary shoot by a marked increase in the level of endogenous cytokinin-like substances and by a decrease in the level of endogenous IAA. By contrast, a significant increase in IAA level and a decreasing trend in the level of cytokinin-like substances occur in the originally inhibited cotyledonary shoot between hour 4 and hour 48 after the release from inhibition of the inhibited cotyledonary shoot. The level of gibberellin-like substances in the cotyledonary shoot released from inhibition steadily increases from the beginning of the release.     

Influence des corrélations entre organes sur la croissance et le développement floral des bourgeons cotylédonaires chez leScrofularia arguta Sol.

The importance of various correlative influences on growth and vegetative or floral development of cotyledonary buds inScrofularia arguta Sol. is shown. The terminal bud, on the one hand, inhibits growth of cotyledonary buds and, on the other hand, induces their early flowering. The cotyledon stimulates growth of its axillary bud, but has no action on its floral development. Leaves above the cotyledonary node have the same effect as the cotyledon. Finally, roots stimulate vegetative growth of cotyledonary buds and suppress floral expression, but only when apical dominance has been removed at an early stage of development.     

Asymmetrical triggering of the cell cycle in opposite buds of a young plant,after a slight cotyledonary wound

Gentle wounding of one cotyledon of a seedling has a rapid, specific and asymmetric effect on the renewal of the cell cycle in the previously quiescent buds at the axil of the cotyledons. Our present experimental system thus may provide a rather simple plant model for studying the complex mechanisms involved in the initiation and termination of the cell cycle in higher plants, in connection with the expression of developmental signals.     

The Architecture of the Stem Apex and the Origin and Development of the Axillary Buds in Seedlings of Acer pseudoplatanus L.

The structure and changes in the size of the stem apex of seedlingsycamores are described. There is no evidence for any regularincrease in size of the apex from pastochrons 6 to 14 inclusive. The formation of the collar by the bases of each pair of foliarprimordia and its association with the formation of axillarybuds has been studied. The first pair of primordia on the axillary bud apex is alwaysat right angles to the axil; the pair of primordia formed inthe plane of the axil are always unequal. On extension growththese axillary buds give rise to lateral shoots which are anisophyllous.An explanation for the anisophylly is offered in terms of thespatial conditions obtaining in the developing axillary bud. The vascularization of the apex is briefly described.     

LEAF-OPPOSED BUDS IN MUSA: THEIR DEVELOPMENT AND A COMPARISON WITH ALLIED MONOCOTYLEDONS

A single, lateral, vegetative bud which is positioned 180° from the axil of a leaf is a generic feature of Musa (Musaceae). Such leaf-opposed buds occur in all ten species and five cultivars examined, representing all four sections of the genus and all groups of cultivated bananas and plantains. The bud arises relatively late and is first visible as a vascular-free “clear zone” in the axis directly below the future bud meristem site. It is first associated with the fifth or sixth leaf primordium from the apex. A defined superficial meristem develops on the stem directly above the insertion of the leaf margins one or more plastochrons later. Normal, basically axillary, vegetative buds occur in the closely related genera: Orchidantha (Lowiaceae), Heliconia (Heliconiaceae), Strelitzia, and Ravenala (Strelitziaceae). These buds arise in the axil of the first to the third leaf primordium in a manner similar to most other monocotyledons. Axillary vegetative buds also occur in the remaining families of the Zingiberales: Cannaceae, Costaceae, Marantaceae, and Zingiberaceae.     

AXILLARY AND DICHOTOMOUS BRANCHING IN THE PALM CHAMAEDOREA

In both Chamaedorea seifrizii Burret and C. cataractarum Martius each adult foliage leaf subtends one axillary bud. The proximal buds in C. seifrizii are always vegetative, producing branches (= new shoots or suckers); and the distal buds on a shoot are always reproductive, producing inflorescences. The prophyll and first few scale leaves of a vegetative branch lack buds. Transitional leaves subtend vegetative buds and adult leaves subtend reproductive buds. Both types of buds are first initiated in the axil of the second or third leaf primordia from the apex, P2 or P3. Later development of both types of bud tends to be more on the adaxial surface of the subtending leaf base than on the shoot axis. Axillary buds of C. cataractarum are similarly initiated in the axil of P2 or P3 and also have an insertion that is more foliar than cauline. However, all buds develop as inflorescences. Vegetative branches arise irregularly by a division of the apex within an enclosing leaf (= P1). A typical inflorescence bud is initiated in the axil of the enclosing leaf when it is in the position of P2 and when each new branch has initiated its own P1. No scale leaves are produced by either branch and the morphological relationship among branches and the enclosing leaf varies. Often the branches are unequal and the enclosing leaf is fasciated. The vegetative branching in C. cataractarum is considered to be developmentally a true dichotomy and is compared with other examples of dichotomous (= terminal) branching in the Angiospermae.     

DEVELOPMENT AND PHYLLOTAXIS OF THE VEGETATIVE AXILLARY BUD OF MICHELIA FUSCATA

Tucker, Shirley C. (Northwestern U., Evanston, III.) Development and phyllotaxis of the vegetative axillary bud of Michelia fuscata . Amer. Jour. Bot. 50(7): 661–668. Illus. 1963.—The vegetative axillary buds of Michelia fuscala are dorsiventrally symmetrical with 2 ranks of alternately produced leaves. The direction of the ontogenetic spiral in each of these buds is related both to the symmetry of the supporting branch and to the position of the bud along the branch. On a radially symmetrical branch, all the axillary buds are alike—all clockwise, for example. But in a dorsiventrally organized branch the symmetry alternates from clockwise in 1 axillary bud to counterclockwise in the next bud along the axis. Leaf initiation and ontogeny of the axillary apical meristem conform with those of the terminal vegetative bud. The axillary bud arises as a shell zone in the second leaf axil from the terminal meristem. During this process the axillary apex develops a zonate appearance. The acropetally developing procambial supply of the axillary bud consists wholly of leaf traces. At the nodal level the bud traces diverge from the same gap as the median bundle trace of the subtending leaf. Only the basal 1–2 axillary buds which form immediately after the flowers elongate each year, while the majority remains dormant with 3 leaves or fewer.     

A COMPARATIVE DEVELOPMENTAL STUDY OF THE MUTANT SIDESHOOTLESS AND NORMAL TOMATO PLANTS

'Sideshootless,’ a mutant strain of tomato which does not produce axillary buds during vegetative growth, was compared with normally branching plants in order to study the nature of development particularly with regard to axillary buds. Sectioned material revealed no indication of axillary bud initiation in the sideshootless plant at any time during the vegetative phase of growth. In the normal plants, buds were noted to arise in the axil of the fifth youngest leaf. The buds take their origin in tissue which is in direct continuity with the apical meristem. The bud primordia later become set apart from the apex as vacuolation takes place in the surrounding tissue. At the time of floral initiation, the mutant and normal strains behave similarly. Axillary buds appear in the axils of the 2 leaves immediately below the floral apex. One of the buds elongates to overtop the existing plant axis; the other develops as a typical sidebranch. The inflorescence is pushed aside in the process. This pattern is repeated with each inflorescence; thus an axis composed of several superimposed laterals results.     

The Influence of Cotyledons in Axillary and Adventitious Shoot Production from Cotyledonary Nodes of Cucumis sativus L. (Cucumber)

Cucumber explants including at least part of the cotyledon,a short section of hypocotyl, and the apical bud, are capableof producing multiple axillary buds from the seedling apex andadventitious shoots from the hypocotyl base in a medium whichcontains 2·0 mg dm^–3 of kinetin. Removal of theapical bud triples the number of shoots produced from the apexof explants with two intact cotyledons but does not affect shootproduction from explants with some or all of their cotyledonsremoved. The area of intact cotyledon also influences morphogenesis,as explants with both cotyledons removed, failed to produceadventitious shoots from the hypocotyl base. Culture in continuousdarkness entirely prevents shoot development from the explantbase, but has little influence on shoot production from theapex. The influence of endogenous growth regulators and apicaldominance on the morphogenesis of shoots in cucumber seedlingsare discussed. Key words: Cucumber, cotyledons, apical dominance, morphogenesis, adventitious shoots, Cucumis sativus     

The role of gibberellins and cytokinins in the growth correlative effect of cotyledons in flax and pea

It is wellknown that following the amputation, or darkening of one cotyledon in decapitated flax seedlings, the opposite remaining, or illuminated, cotyledon exerts a stimulatory effect on the growth of its axillary bud. For the induction of this stimulating effect a 21–72 h continuous darkening of the cotyledon is sufficient. Endogenous gibberellins take part in the stimulation effect of the illuminated cotyledon, since their level in the illuminated cotyledon increases as early as 12–48 h following the darkening of the opposite cotyledon. The apical part of the cotyledon has a higher growth stimulatory effect on the growth of the cotyledonary axillary bud than the basal half. This again is associated with endogenous gibberellins the level of which is higher in the apical half of the cotyledon than in the basal one. Upon removal of the root and hypocotyl base in decapitated flax seedlings deprived of one cotyledon, the remaining cotyledon loses its stimulatory influence, so that the bud of the amputated cotyledon grows more vigorously (Dostál 1955). In this growth correlative phenomenon the root may be substituted by cytokinin BA applied in the form of a 0.1–1.0 per cent paste onto the remaining cotyledon, for again in this case the bud of the preserved cotyledon grows more vigorously. Following the decapitation of the axillary of the amputated cotyledon in decapitated pea seedlings with an intact root and deprived of one cotyledon, the axillary of the remaining cotyledon grows more intensively than the serial of the removed one. If the plants operated on in the same way are deprived of the root, the serial of the removed cotyledon gains a correlative growth predominance. If the plants deprived of root are cultivated at the same time in a solution of BA (10–20 mg 1⁻¹), the correlative predominance is acquired by the axillary of the remaining cotyledon. In growth correlations between cotyledons and their axillary buds in pea seedlings the root may thus be substituted by exogenous cytokinin, as well.     

LIGNOTUBER ONTOGENY IN THE CORK-OAK (QUERCUS SUBER; FAGACEAE) I. LATE EMBRYO

Changes at the cotyledonary node of the cork-oak (Quercus suber L.) were examined during the embryo maturation phase using light microscopy and scanning electron microscopy techniques. During the maturation phase the embryo axis elongates by diffuse growth, the apical meristem forms the first leaf primordia, and the radicle meristem remains inactive. The primary axis of the embryo bears, axillary to the cotyledons, in the range of five to seven pairs of lateral buds at differing stages of development. Two or three pairs of these buds are visible, occurring on the upper unfused portion of the embryonic axis, while the remaining buds are hidden by the fused cotyledonary tissues. Lateral buds develop from clusters of cells in the peripheral meristem forming a shell zone delimiting the bud meristem. Lateral buds do not undergo much development until germination begins. The results are discussed with reference to the possible role of the cotyledonary node as the source of the lignotuber in the cork-oak.