An Automata-theoretical Model of Meristem Development as Applied to the Primary Root of Zea mays L.

Observations were made of the sequence of division within thecellular packets (groups of cells of common descent) which comprisethe cell files that run the length of the central cortex ofthe primary root meristem ofZea mays. These sequences, and alsothe relative lengths of the cells within the packets recordedat various times during root growth, indicate that cell-filedevelopment can be expressed using one, or a limited number,of deterministic ‘bootstrap’ L-systems which assigndifferent lifespans to sister cells of successive cell generations.The outcome is a regular pattern of divisions from which daughtercells emerge usually with unequal, but definite, lengths. Inthe immediately post-germination stage of root growth, one divisionpathway is especially common in the cortex and generates sequencesof unequal daughters having a particular basi-apical orientation.Later in root growth, the cellular pattern in the cortex indicatesthat this pathway is replaced by another where unequal divisionsare not so marked, but which nevertheless continues to maintaina regular arrangement of differently sized cells. This latterpathway is characteristic of a zone close to the initial cellsof the cortex. It is present at all stages of root growth andspreads along the length of the cortex as the descendants ofthese initials proliferate. The development of the whole corticalcell file can be simulated from knowledge of the growth functionsof the bootstrap systems. The files so generated contain allthe observed cell patterns. The growth functions also predictthe sequence in which cells cease dividing near the proximalmargin of the meristem, but for this it is necessary to incorporatea counter for the number of divisions that will be accomplishedin the cell file. Cytological requirements for the propagationof unequal divisions, together with a consideration of the natureof the division counter, as well as the significance of theswitch in division pathways encountered during early root growth,are discussed in the context of this deterministic model ofcell division. Cell division; root meristem; L-systems; Zea mays     

Deterministic Patterns of Cellular Growth and Division Within a Meristem

The primary root meristem of maize (Zea mays L.) is composedof longitudinal files of cells arranged in groups of familialdescent (sisters, cousins, etc.). In the proximal portion ofthe meristem, the cells in these groups, or packets, show orderedsequences of division that are transverse with respect to theapico-basal axis of the root. The division sequences fall intoa relatively small number of pathways which can be describedusing deterministic 'bootstrap' L-systems. Although these systemscan operate through the assignment of determinate lifespansto sister cells which thus specify their subsequent interdivisionalperiod, because of their exponential growth kinetics the systemscan also operate with determinate units of cell extension. Thisdeterministic type of system allows simulation not only of thedivision sequences, but also of the lengths of the cells thatare present within the packets which participate in the differentdivision pathways. The types of L-systems used to describe thesepathways also predict the distributions and ranges of cell andpacket lengths found after varying numbers of cell generations.These distributions compare favourably with those actually foundin the maize root meristem. Theoretical aspects of bootstrapL-systems, essential for their application to the one-dimensionalcellular arrays of the meristematic cell-files of the maizeroot apex, are also presented.Copyright 1994, 1999 AcademicPress Cell division, cell elongation, cell polarity, L-system, root meristem, Zea mays     

Rhythmic plant morphogenesis: Recurrent patterns of idioblast cell production

Most plants are constructed from repeating modular units such as phytomers, merophytes, and cell packets. Even an organism as simple as the filamentous cyanobacterium Anabaena shows recurrent patterns of differentiated cellular structures, notably with respect to its heterocysts. These examples reflect the inherent rhythms established within developmental processes of living organisms. In the present article, attention is paid to repetitious production of idioblasts—isolated cells, or clusters of cells, with an identity different to that of neighbouring cells from which they are derived. In higher plant root tissues, idioblasts are contained within cell packets that grow up from mother cells during the course of a number of cycles of cell production. The heterocysts of Anabaena are also discussed; they, too, are a type of idioblast. The idioblasts of root tissues originate as small cells which result from unequal cell divisions. Such divisions are usually the final ones within a cell packet which has already undergone a number of division cycles and are characteristically located at one or both ends of a packet. The packet end walls are suggested to have a role in regulating division asymmetry. Idioblastic systems discussed are root cortical trichosclereids and diaphragm cells; in their earliest stage, the cells from which lateral root primordia arise are also considered as clusters of idioblasts because they, too, are the products of asymmetric divisions of pericyclic mother cells. The division patterns of all these idioblastic systems were modelled in a consistent way using L-systems, with the assumption that the age of a cell-packet end wall plays a special role in cell determination. This article is dedicated to Vsevelod Ya. Brodsky, doyen of Russian studies of rhythms in cell division and development, who celebrates his 80th birthday on August 4, 2008 This article was presented in original.     

Clonal analysis of the Arabidopsis root confirms that position, not lineage, determines cell fate

 The cellular organization of the Arabidopsis thaliana (L.) Heynh. root meristem suggests that a regular pattern of cell divisions occurs in the root tip. Deviations from this pattern of division might be expected to disrupt the organization of cells and tissues in the root. A clonal analysis of the 3-d-old primary root meristem was carried out to determine if there is variability in division patterns, and if so to discover their effect on cellular organization in the root. Clones induced in the seedling meristem largely confirmed the predicted pattern of cell divisions. However, the cellular initials that normally give rise to the different cell files in the root were shown to exhibit some instability. For example, it was calculated that a lateral root cap/epidermal initial is displaced every 13 d. Furthermore, the existence of large marked clones that included more than two adjacent cell layers suggests that intrusive growth followed by cell division may occur at low frequency, perhaps in response to local cell deaths in the meristem. These findings support the view that even in plant organs with stereotypical cell division patterns, positional information is still the key determinant of cell fate. Received: 27 August 1999 / Accepted: 4 December 1999     

Time-lapse analysis of stem-cell divisions in the Arabidopsis thaliana root meristem

In the Arabidopsis root, asymmetric stem-cell divisions produce daughters that form the different root cell types. Here we report the establishment of a confocal tracking system that allows the analysis of numbers and orientations of cell divisions in root stem cells. The system provides direct evidence that stem cells have lower division rates than cells in the proximal meristem. It also allows tracking of cell division timing, which we have used to analyse the synchronization of root cap divisions. Finally, it gives new insights into lateral root cap formation: epidermal stem-cell daughters can rotate the orientation of the division plane like the stem cell.     

Cell division patterns of the protoderm and root cap in the “closed” root apical meristem ofArabidopsis thaliana

Summary The peripheral root cap and protoderm inArabidopsis thaliana are organized into modular packets of cells derived from formative T-divisions of the root cap/protoderm (RCP) initials and subsequent proliferative divisions of their daughter cells. Each module consists of protoderm and peripheral root cap packets derived from the same periclinal T-division event of an RCP initial. Anatomical analyses are used to interpret the history of extensively coordinated cell divisions producing this modular construction. Within a given layer of root cap, the columella and RCP initials divided in a centrifugal sequence from the innermost columella initials toward the RCP initials. All RCP initials in the lineages around the circumference of the root divided nearly simultaneously in waves to form one module prior to the next wave of initial divisions forming a younger module. The peripheral root cap and protoderm packets within each module completed four rounds of proliferative divisions in the axial plane to produce, on average, 16 cells per packet in the basalmost modules in axial view. Peripheral root cap and protoderm cells predominantly in the T-type (trichoblast) lineages also underwent radial divisions as they were displaced basipetally. The regularity in the cellular pattern within the modules suggests a timing mechanism controlling highly coordinated cell division in the initials and their daughter cells.Abbreviations RAM root apical meristem - RCP root cap protoderm - prc peripheral root cap     

Meristem as a Self-Renewing System: Maintenance and Cessation of Cell Proliferation (A Review)

The mechanisms of the maintenance of long-term cell proliferation and its cessation in the meristem of the growing root were analyzed. Quiescent center (QC) remains in the meristem for a long time, whereas all other cells leave the meristem after several mitotic cycles. The question arises as to what extent such organization of proliferation corresponds to the concept of stem cells elaborated for animals. The definition of animal stem cells is met by the QC cells rather than by actively dividing cells that boundary it. However, QC is not a self-maintaining population of cells originated during early stages of embryogenesis; it is formed from dividing cells in the main or lateral root. After root decapitation, the QC can arise from the cells that normally would leave the meristem before long. There is a zone of the meristem whose cells are capable of remaining and forming QC after the removal of the apical part of the root. Maintenance of the size of the meristem depends on the interaction between QC, initial cells located at its surface, and the actively dividing cells. Apparently, the life span of cells in the meristem determines the time when the meristematic cell will begin the elongation. The number of cells starting the elongation depends on proliferation rate and on the changes in life span of meristematic cells which determine their initial number. The life span of the cells in the meristem for most actively dividing cells does not depend on the cell divisions, and remains unchanged in the presence of various inhibitors. As a result of inhibited proliferation in the main part of the meristem, cell divisions in the QC are activated and newly formed cells may proceed to rapid divisions. Thus, the size of the meristem is maintained by the operation of several mechanisms, and individual processes may be, on the one hand, relatively independent and, on the other hand, regulated either by feedback or directly. As a result, the root growth becomes resistant to various external events.     

Experimental Modification of Cell Division Patterns in the Root Meristem of Zea mays

In the meristem of the young primary root of maize seedlingsthe first transverse division in the cortex 250 µm fromthe root apex results in two daughter cells of distinctly unequalsize. This division could be rendered equal by raising the seedlingsin up to 7.5% methanol. The pattern of the subsequent two orthree transverse divisions in the cortex, as revealed by thearrangement of the newly divided cells in the resultant cellularpackets, was acropetal in the methanol-treated roots but basipetalin the control roots. The sequence of division within a cellularpacket tended to follow the distribution of cell sizes - largercells divided earlier than smaller cells. A temporary arrestof cell division by exposing roots to cold (5 °C) conditionshad no effect on the sequence of divisions that followed whenthe roots were allowed to recover at 20 °C. The resultssuggest that the normally asymmetric position of the cell wallformed at cytokinesis is subject to active regulation and thatmethanol interferes with this process. The cytoplasm of certaincells in the root meristem was also found to be unequally distributed,as judged by Azure B staining, between the two ends of the cell.Cytoplasmic asymmetry was not directly correlated with inequalityof division, although it too was affected by methanol. Cell polarity, root meristem, unequal division, Zea mays     

Properties of plate meristem of growing epigeal cotyledons in an experimental system

Plate meristem activity in epigeal cotyledons of plants, which are largely used in research, was comparatively studied. Formation of growing clusters of daughter cells is a common feature of cotyledon meristems. Species-specific differences connected with the number of cells entering division, the homogeneity of the palisade cell population, tissue specification of proliferation, the end number of daughter cells in clusters and the possibility to use clusters for simultaneous determination of the cell growth and division activity are shown. Exogenous cytokinin enlarges the number of cells entering proliferative divisions in the division competent tissues of the respective cotyledon and stimulates the growth of isolated cotyledons cultured in darkness. The analysis of morphological peculiarities substantiates the properties of the meristems of studied species in an experimental system and the possible light microscopy approach for using them in obtaining data on the number of divisions and accompanying cell growth. The first palisade layer of zucchini cotyledon was chosen as the most suitable experimental system reflecting the cellular behaviour during the growth of a plant organ and permitting easy and exact quantification of the cell divisions and growth simultaneously.     

Tissue-6

In order to study a possible involvement of cdc-like proteinkinases in cell development and tissue differentiation, a polyclonalantibody raised against the evolutionary conserved PSTAIR-regionof p34^cdc2-homologue protein kinases (PSTAIR-proteins) was appliedto sections of the maize root apices. PSTAIR-proteins were localizedin the nuclei and the cytoplasm of cells in the root meristem,including the quiescent centre (QC), and of all dividing cellsthat form the lateral root primordia. In most root tissues,the amount of cytoplasmic PSTAIR-proteins progressively declinedwith increasing distance from the root cap junction, becomingrestricted to the nucleus after the cessation of cell divisions.This occurred much nearer to the root cap junction in cellsof the stele, especially in metaxylem cells, than in cells ofthe root cortex. Interesting exceptions were cells of the pericycle,endodermis and the outermost cell rows of stelar parenchyma,which exhibited relatively high levels of the cytoplasmic PSTAIR-proteinsthroughout all developmental zones. After root wounding, rapid cytoplasmic accumulation of PSTAIR-proteinsin cells adjacent to the wound was observed in all tissues ofthe meristem and of the elongation zone. This wound response,which was usually followed by newly-induced cell divisions,was delayed with increasing distance from the root cap junctionin a tissue-specific manner. Since PSTAIR-proteins were foundin the cell nuclei throughout all developmental zones, theyseem to have some nuclear functions which continue even aftercell division has stopped. Key words: Cell cycle, maize roots, cyclin-dependent protein kinases, wounding     

Developmental pattern formation of somatic embryos induced in cell suspension cultures of cowpea [Vigna unguiculata (L.) Walp]

The sequence of events in the functional body pattern formation during the somatic embryo development in cowpea suspensions is described under three heads. Early stages of somatic embryogenesis were characterized by both periclinal and anticlinal cell divisions. Differentiation of the protoderm cell layer by periclinal divisions marked the commencement of somatic embryogenesis. The most critical events appear to be the formation of apical meristems, establishment of apical-basal patterns of symmetry, and cellular organization in oblong-stage somatic embryo for the transition to torpedo and cotyledonary-stage somatic embryos. Two different stages of mature embryos showing distinct morphology, classified based on the number of cotyledons and their ability to convert into plantlets, were visualized. Repeated mitotic divisions of the sub-epidermal cell layers marked the induction of proembryogenic mass (PEM) in the embryogenic calli. The first division plane was periclinally-oriented, the second anticlinally-oriented, and the subsequent division planes appeared in any direction, leading to clusters of proembryogenic clumps. Differentiation of the protoderm layer marks the beginning of the structural differentiation in globular stage. Incipient procambium formation is the first sign of somatic embryo transition. Axial elongation of inner isodiametric cells of the globular somatic embryo followed by the change in the growth axis of the procambium is an important event in oblong-stage somatic embryo. Vacuolation in the ground meristem of torpedo-stage embryo begins the process of histodifferentiation. Three major embryonic tissue systems; shoot apical meristem, root apical meristem, and the differentiation of procambial strands, are visible in torpedo-stage somatic embryo. Monocotyledonary-stage somatic embryo induced both the shoot apical meristem and two leaf primordia compared to the ansiocotyledonary somatic embryo.     

Tissue- and development-specific distributions of cytoskeletal elements in growing cells of the maize root apex

ABSTRACT

Indirect immunofluorescence performed using sections of actively growing maize root apices fixed and then embedded in low-melting-point Steedman's wax has proved efficient in revealing the arrangements and reorganizations of motility-related cytoskeletal elements which are associated with root cell development and tissue differentiation. This powerful, yet relatively simple, technique shows that specific rearrangements of both microtubular (MT) and actin microfilament (MF) arrays occur in cells as they leave the meristem and traverse the transitional region interpolated between meristem and elongation region. Cytoskeletal and growth analyses have identified the transition zone as critical for both cell and root development; it is in this zone that cell growth is channelled, by the cytoskeleton, into a strictly polarized mode which enables root tips to extend rapidly through the soil in search of water and nutrients. An integrated cytoskeletal network is crucial for both the cytomorphogenesis of individual cells and the overall morphogenesis of the plant body. The latter process can be viewed as a reflection of the tight control which cytoskeletal networks exert not only over cell division planes in the cells within meristematic apices but also over the orientation of cell growth in the meristem and elsewhere. Endoplasmic MTs interconnecting the plasma membrane with the nucleus are suggested to be involved in cell division control; they may also act as a two-way cytoskeletal communication channel for signals passing to and fro between the extracellular environment and the genome. Moreover, the dynamism of endoplasmic MTs exerts direct effects on chromatin structure and the accompanying nuclear architecture and hence can help exert a cellular level of control over cell growth and cell cycle progression. Because the inherent dynamic instability of MTs depends on the concentration of tubulin dimers within the cytoplasm, we propose that when asymmetric cell division occurs, it will result in two daughter cells which differ in the turnover rates of their MTs. This phenomenon could be responsible for different cell fates of daughter plant cells produced by such cell divisions.     

Two ways to skin a plant: The analysis of root and shoot epidermal development in Arabidopsis

The post-embryonic architecture of higher plants is derived from the activity of two meristems that are formed in the embryo: the shoot meristem and the root meristem. The epidermis of the shoot is derived from the outermost layer of cells covering the shoot meristem through repeated anticlinal divisions. By contrast, the epidermis of the root is derived from an internal ring of cells, located at the centre of the root meristem, by a precise series of both periclinal and anticlinal divisions. Each epidermis has an independent origin. In Arabidopsis the mature shoot epidermis is composed of a small number of cell types: hair cells (trichomes), stomatal guard cells and other epidermal cells. In shoots, hairs take the form of branched trichomes that are surrounded at their base by a ring of accessory cells in a sheet of epidermal cells. The root epidermis is composed of two cell types: trichoblasts that form root hair cells and atrichoblasts that form non-hair cells. Mutations affecting both the patterning and the morphogenesis of cells in both shoot and root epidermis have recently been described. Most of these mutations affect development in a single epidermis, but at least one, ttg, is involved in development in both epidermal systems.     

Cell division patterns in the apices of subterranean axis and aerial shoot of Psilotum nudum (Psilotaceae): morphological and phylogenetic implications for the subterranean axis

The cell division pattern in the apical meristem of Psilotum nudum was examined using epi-illumination microscopy and a paraffin method. In the subterranean axis, about half of the derivative cells of the apical cell produce tetrahedral daughter apical cells by the first three or more oblique divisions. Roughly half of these apical cells give rise to the apical meristems of axes, whereas the other half do not. Various relative activities of the mother and daughter apical cells give rise to disordered branching patterns. In the ill-organized apical meristem as well as the leafless and capless structure, the Psilotum subterranean axis differs from the basic organs of vascular plants such as stem and root and seems to be an independent organ. The cell division pattern characteristic of the subterranean axis persists in the young unbranched aerial shoots, although fewer daughter apical cells are produced. Dichotomous branching of the aerial shoots, as in a variety of organs of pteridophytes, involves loss of the mother apical cell followed by appearance of two daughter apical cells.     

What the Distribution of Cell Lengths in the Root Meristem Does and Does Not Reveal About Cell Division

Roots have long been realized to be useful material for studies of cell division. Despite this long history of use, the behavior of cells in the meristem is often misinterpreted. A common error is to argue that differences in cell length reflect differences in cell division rate. In this article we explain the fallacy behind this argument and show how the analysis of cell length distribution can lead to insight about the root meristem. These observations support a model for the root meristem where cells of various tissues grow at the same relative growth rate and divide at the same frequency, indicating that these growth parameters are built into the cells at a fundamental level. The differences in cell length between various tissues appear to arise at their formation, first at the tissue initials and ultimately in the seed. Length differences among mature cells may be enhanced by differences in the location within the meristem where division ceases. Discovering mechanisms regulating the length of initial cells and the position where cells cease division requires a realistic understanding of how growth constrains the division behavior of dividing cells.     

SCHIZORIZA controls an asymmetric cell division and restricts epidermal identity in the Arabidopsis root

The primary root of Arabidopsis has a simple cellular organisation. The fixed radial cell pattern results from stereotypical cell divisions that occur in the meristem. Here we describe the characterisation of schizoriza (scz), a mutant with defective radial patterning. In scz mutants, the subepidermal layer (ground tissue) develops root hairs. Root hairs normally only form on epidermal cells of wild-type plants. Moreover, extra periclinal divisions (new wall parallel to surface of the root) occur in the scz root resulting in the formation of supernumerary layers in the ground tissue. Both scarecrow (scr) and short root (shr) suppress the extra periclinal divisions characteristic of scz mutant roots. This results in the formation of a single layered ground tissue in the double mutants. Cells of this layer develop root hairs, indicating that mis-specification of the ground tissue in scz mutants is uncoupled to the cell division defect. This suggests that during the development of the ground tissue SCZ has two distinct roles: (1) it acts as a suppressor of epidermal fate in the ground tissue, and (2) it is required to repress periclinal divisions in the meristem. It may act in the same pathway as SCR and SHR.     

Asymmetric cell division and cell fate in plants

A variety of approaches has recently been employed to investigate how sister cells adopt distinct fates following asymmetric divisions during plant development. Surgical and drug studies have been used to analyze asymmetric divisions during both early embryogenesis in brown algae and pollen development in tobacco. Genetic screens have been used to identify genes in Arabidopsis thaliana that are required for specific asymmetric cell divisions during pollen and root development. These studies indicate that cell polarity and division orientation are closely tied to the process of cell fate specification, and suggest that differential inheritance of determinants and positional information may both be involved in the specification of cell fates following asymmetric cell division.