The Principles of Data Formalization for Building Biological Model of Shoot Development in Flowering Plants

Shoot system of a plant can be divided into elementary molecules composed of phyllome, internode, and meristem of the lateral bud. The capacity of plants for open growth is manifested as multiple reproductions of the modules. These main principles of plant structural organization can be used to formalize and integrate the data from various disciplines studying shoot development—genetics of development, morphology, etc. At the example of a model species Arabidopsis thaliana we show that the data on genetic control of shoot development can be considered in terms of rearrangement of individual modules. Several variants of the module structural reorganization are allowed: reduction or transformation of phyllome, change in the internode length, and triggering active/inactive status of the lateral shoot meristem. Each variant of module structure corresponds to specific pattern of genes activity. Such integration of the data on genetic and structural aspects of morphogenesis can form a basis for mathematical modeling of plant development.     

Growth rhythms at different stages of shoot morphogenesis in woody plants

Research data on the rhythms of shoot growth in woody plants obtained in the second half of the 20th century are reviewed. Analysis of these data demonstrated different regulation of shoot growth processes at three stages of its development: (1) initiation of shoot primordia, (2) primordia development into phyllome primordia, and (3) visible shoot growth. The growth rhythm after the first stage was realized at the level of apical shoot meristem; at the second stage, at the individual shoot level; and at the third stage, at the whole plant level.     

Growth rhythms at different stages of shoot morphogenesis in woody plants

Research data on the rhythms of shoot growth in woody plants obtained in the second half of the 20th century are reviewed. Analysis of these data demonstrated different regulation of shoot growth processes at three stages of its development: (1) initiation of shoot primordia, (2) primordia development into phyllome primordia, and (3) visible shoot growth. The growth rhythm after the first stage was realized at the level of apical shoot meristem; at the second stage, at the individual shoot level; and at the third stage, at the whole plant level.     

Significance of the simultaneous growth of vegetative and reproductive organs in the prostrate annual Chamaesyce maculata (L.) Small (Euphorbiaceae)

To elucidate the significance of the simultaneous growth of vegetative and reproductive organs in the prostrate annual Chamaesyce maculata (L.) Small (Euphorbiaceae) from the standpoint of meristem allocation, we investigated plant architecture, meristem allocation, and the spatial and temporal patterns in vegetative growth and reproduction in the reproductive stage. The numbers of secondary and tertiary shoots successively increased by branching in the reproductive stage, and the sum of shoot length was greater in secondary shoots than in primary shoots. The specific shoot length (shoot length per shoot biomass) was greater in lateral shoots than in primary shoots, indicating efficient lateral shoot elongation. The internode length was shorter in secondary shoots than in primary shoots, increasing the number of nodes per shoot length in secondary shoots. Many nodes on a shoot generated two meristems, one of which committed to a flower and one to a lateral shoot. The number of reproductive meristems was greatest in tertiary shoots, and 96% of total reproductive meristems on shoots were generated in lateral shoots. On almost all nodes, the reproductive meristem developed into a flower, and 95–98% of the flowers produced a fruit. Therefore, vegetative growth by branching in the reproductive stage contributed to the increase in reproductive outputs. From the standpoint of meristem allocation, the simultaneous growth of vegetative and reproductive organs in prostrate plant species might be important for increasing the number of growth and reproductive meristems, resulting in the increase in reproductive outputs.     

A new conception of the shoot of higher plants

According to the classical model, the “shoot” consists only of the categories “caulome” (“stem” sensu lato) and “phyllome” (“leaf” sensu lato), (and “root” in cases of “adventitious” root formation). If lateral shoots are present, their position is axillary. Consequently, caulome as well as phyllome are inserted on the caulome and only on the caulome. This classical model of the shoot has two disadvantages of great consequence: (1) Intermediate organs cannot be accepted as such, but have to be interpreted (i.e. categorized) as either caulome or phyllome (or root) by distortion of the actual similarity. (2) Certain positional changes of organs cannot be accepted as such, but have to be “explained” by congenital fusion. The new conception of the shoot will have the advantages of the classical model but not its disadvantages. Hence, the shoot may consist of the following parts: (main and lateral) shoot, caulome, phyllome, root, emergence, and structures intermediate between (i.e. partially homologous to) any of the preceding. Thus, the five categories of the classical model, namely “shoot”, “caulome”, “phyllome”, “root” and “emergence” are no longer mutually exclusive; they may merge into each other due to an actual or potential continuum. Intermediate organs are therefore accepted as such; for example, an organ may be characterized as an intermediate form between a caulome and a phyllome. Besides intermediate forms, all changes in position are accepted as such. Hence, the following positional relations are possible: caulome and phyllome may be inserted on the caulome, caulome and phyllome may be inserted on the phyllome; roots may be inserted on caulome or phyllome; intermediate forms may be inserted on the caulome, phyllome, or other intermediate forms. Consequences of the new conception for morphological research are pointed out, especially for homologization, evolutionary considerations, and the direction in which research progresses.     

Cell-lineage patterns in the shoot apical meristem of the germinating maize embryo

A fate map for the shoot apical meristem of Zea mays L. at the time of germination was constructed by examining somatic sectors (clones) induced by -rays. The shoot apical meristem produced stem, leaves, and reproductive structures above leaf 6 after germination and the analysis here concerns their formation. On 160 adult plants which had produced 17 or 18 leaves, 277 anthocyanin-deficient sectors were scored for size and position. Sectors found on the ear shoot or in the tassel most often extended into the vegetative part of the plant. Sectors ranged from one to six internodes in length and some sectors of more than one internode were observed at all positions on the plant. Single-internode sectors predominated in the basal internodes (7,8,9) while longer sectors were common in the middle and upper internodes. The apparent number of cells which gave rise to a particular internode was variable and sectors were not restricted to the lineage unit: a leaf, the internode below it, and the axillary bud and prophyll at the base of the internode. These observations established two major features of meristem activity: 1) at the time of germination the developmental fate of any cell or group of cells was not fixed, and 2) at the time of germination cells at the same location in a meristem could produce greatly different amounts of tissue in the adult plant. Consequently, the developmental fate of specific cells in the germinating meristem could only be assigned in a general way.Abbreviations ACN apparent cell number - LI, LII, LI-LII sectors restricted to the epidermis, the subepidermis, or encompassing epidermis and subepidermis - PCN progenitor cell     

THE SHELL ZONE: ITS DIFFERENTIATION AND PROBABLE FUNCTION IN SOME DICOTYLEDONS

Thirty-five species belonging to various dicotyledonous families were investigated to study the origin, development, and probable function of the shell zone, which is defined as an arcuate zone of cambiform cells delimiting the early axillary bud meristem. It is present in the majority of the investigated plants and five intergrading patterns of origin are described: (i) from the parenchymatized derivatives of the cells of the peripheral meristem of the shoot apex, adaxial to the bud meristem, (ii) from the peripheral meristem of the shoot apex along with the initiation of the early bud meristem, (iii) from the adaxial cells of the bud meristem, (iv) from the derivatives of the cells of the bud meristem at its base, and (v) partly from the parenchymatized cells of the peripheral meristem adaxial to the bud and partly from the adaxial derivatives of the bud meristem. The shell zone loses its identity at different stages of bud development in various species. Its cells ultimately contribute to the ground meristem, procambium, and pith cells of the axis. In Cuminum cyminum and lpomoea cairica the shell zone contributes in bringing about the axillary position of the bud from its early lateral position. In Solarium melongena, derivatives of the shell zone initiate the internodal elongation between the flower or inflorescence and the shoot apex, ultimately shifting the bud to an extra-axillary position on the internode.     

Developmental control of cell division patterns in the shoot apex

The shoot apical meristem is a group of rapidly dividing cells that generate all aerial parts of the plant. It is a highly organised structure, which can be divided into functionally distinct domains, characterised by specific proliferation rates of the individual cells. Genetic studies have enabled the identification of regulators of meristem function. These factors are involved in the formation and maintenance of the meristem, as well as in the formation of the primordia. Somehow, they must also govern cell proliferation rates within the shoot apex. Possible links between meristem regulators and the cell cycle machinery will be discussed. In order to analyse the role of cell proliferation in development, cell cycle gene expression has been perturbed using transgenic approaches and mutation. The effect of these alterations on growth and development at the shoot apex will be presented. Together, these studies give a first insight into the regulatory networks controlling the cell cycle and into the significance of cell proliferation in plant development.     

Meristems, metamers and modules and the development of shoot and root systems

BARLOW, P. W., 1989. Meristems, metamers and modules in the development of shoot and root systems . Root and shoot systems are hierarchical organizations whose levels are represented, in part, by cells and meristems. Meristems produce modules which in turn construct the architectural model. The latter is species specific and its structure depends on the geometrical interrelationships between the modular elements. The place of the metamer within this hierarchical scheme is discussed. Metamers derive directly from meristem activity and are externally recognizable as reiterated sub-units of the module. Another sub-unit of module construction, the cellular complex, or merophyte, is also a product of meristem activity, but, in contrast to the metamer, it is an internal, rather than an external, anatomical feature. Being cellular, it increases the ‘span’ of the cell level rather than constituting a level in its own right. Although the physical boundaries of metamer and merophyte can overlap, or even coincide, the two units belong to different conceptual schemes of module structure: the metamer is defined from a ‘classical’ morphological viewpoint, whereas the merophyte derives from a cellular conception of plant structure. Both the merophyte and the metamer have a role in clarifying the understanding of plant development since both provide insights into the functioning of the meristems from which they are derived and the structure of the module to which they contribute. For example, modules which lack an obvious metameric construction can usefully be analysed in terms of their merophytic organization. This is particularly true of roots of lower plants. Here, the merophytes reflect the presence and activity of a specialized meristematic apical cell. On the other hand, modules of higher plants, which lack such apical cells, also lack clearly defined merophytes, but their shoots have obvious metamers which reflect the activity of the meristem as a whole. It should be possible to represent the development of modules from cells, via their intermediate sub-structures of meristems and metamers, by means of formal languages of automata theory. One of these, a graphical algorithm (Petri net), is applied in this developmental context.     

A Relationship between Gibberellic Acid and Light in the Control of Internode Extension of Dwarf Peas (Pisum sativum)

Experimental evidence indicates that gibberellic acid (GA) hasan insignificant effect on the internode growth-rate in dwarfpeas germinated and grown in darkness. When exposed to eitherred or white light and treatment with GA, dwarf pea seedlingsshow marked internode extension. Various combinations of lightand dark together with GA indicate the possibility of the formationof a light-promoted growth inhibitor which can be reversed inits action by GA. It is suggested that the site for interactionof the postulated inhibitor and exogenous GA is immediatelyadjacent to the shoot meristem.     

Branching Shoots and Spikes from Lateral Meristems in Bread Wheat

Wheat grain yield consists of three components: spikes per plant, grains per spike (i.e. head or ear), and grain weight; and the grains per spike can be dissected into two subcomponents: spikelets per spike and grains per spikelet. An increase in any of these components will directly contribute to grain yield. Wheat morphology biology tells that a wheat plant has no lateral meristem that forms any branching shoot or spike. In this study, we report two novel shoot and spike traits that were produced from lateral meristems in bread wheat. One is supernumerary shoot that was developed from an axillary bud at the axil of leaves on the elongated internodes of the main stem. The other is supernumerary spike that was generated from a spikelet meristem on a spike. In addition, supernumerary spikelets were generated on the same rachis node of the spike in the plant that had supernumerary shoot and spikes. All of these supernumerary shoots/spikes/spikelets found in the super wheat plants produced normal fertility and seeds, displaying huge yield potential in bread wheat.     

Simulation of organ patterning on the floral meristem using a polar auxin transport model

An intriguing phenomenon in plant development is the timing and positioning of lateral organ initiation, which is a fundamental aspect of plant architecture. Although important progress has been made in elucidating the role of auxin transport in the vegetative shoot to explain the phyllotaxis of leaf formation in a spiral fashion, a model study of the role of auxin transport in whorled organ patterning in the expanding floral meristem is not available yet. We present an initial simulation approach to study the mechanisms that are expected to play an important role. Starting point is a confocal imaging study of Arabidopsis floral meristems at consecutive time points during flower development. These images reveal auxin accumulation patterns at the positions of the organs, which strongly suggests that the role of auxin in the floral meristem is similar to the role it plays in the shoot apical meristem. This is the basis for a simulation study of auxin transport through a growing floral meristem, which may answer the question whether auxin transport can in itself be responsible for the typical whorled floral pattern. We combined a cellular growth model for the meristem with a polar auxin transport model. The model predicts that sepals are initiated by auxin maxima arising early during meristem outgrowth. These form a pre-pattern relative to which a series of smaller auxin maxima are positioned, which partially overlap with the anlagen of petals, stamens, and carpels. We adjusted the model parameters corresponding to properties of floral mutants and found that the model predictions agree with the observed mutant patterns. The predicted timing of the primordia outgrowth and the timing and positioning of the sepal primordia show remarkable similarities with a developing flower in nature.     

The shoot meristem as a site of continuous organogenesis

In higher plants, organ formation occurs throughout life. This remarkable process occurs at a collection of stem cells termed the shoot meristem. The shoot meristem originates during embryogenesis and is later responsible for generating the above-ground portion of the plant. The shoot meristem can be thought of as having two zones, a central zone containing meristematic cells in an undifferentiated state, and a surrounding peripheral zone where cells enter a specific developmental pathway toward a differentiated state. Recent advances have revealed several genes that specifically regulate meristem development inArabidopsis. The function of these genes and their genetic interactions are described.     

Identifying novel regulators of shoot meristem development

New organs are initiated throughout the life span of higher plants. This process occurs at the shoot meristem, which is initiated during embryogenesis and is later responsible for generating the above-ground portion of the plant. The shoot meristem can be thought of as having two zones, a central zone containing meristematic cells in an undifferentiated state, and a surrounding peripheral zone where cells enter a specific developmental pathway toward a differentiated state. Recent advances have revealed several genes that specifically regulate meristem development inArabidopsis. However, extensive mutagenesis by several labs have identified only a handful, of loci that appear to specifically regulate shoot meristem development. We have undertaken an enhancer/suppressor mutagenesis of an existing meristem mutant (clv1) and have identified novel regulators of meristem development. The extended abstract of a paper presented at the 13th International Symposium in Conjugation with Award of the International Prize for Biology “Frontier of Plant Biology”     

Auxin: A major regulator of organogenesis

Plant development is characterized by the continuous initiation of tissues and organs. The meristems, which are small stem cell populations, are involved in this process. The shoot apical meristem produces lateral organs at its flanks and generates the growing stem. These lateral organs are arranged in a stereotyped pattern called phyllotaxis. Organ initiation in the peripheral zone of the meristem involves accumulation of the plant hormone auxin. Auxin is transported in a polar way by influx and efflux carriers located at cell membranes. Polar localization of the PIN1 efflux carrier in meristematic cells generates auxin concentration gradients and PIN1 localization depends, in turn, on auxin gradients: this feedback loop generates a dynamic auxin distribution which controls phyllotaxis. Furthermore, PIN-dependent local auxin gradients represent a common module for organ initiation, in the shoot and in the root.