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Transformations of Cellular Pattern: Progress in the Analysis of Stomatal Cellular Complexes Using L-Systems

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Progress in Botany 71

Part of the book series: Progress in Botany ((BOTANY,volume 71))

Abstract

Stomatogenesis involves a progressive transformation of selected protodermal cells on primary plant tissue surfaces, especially those of leaves, and culminates in the formation of a functional stomatal apparatus. The transformations are accompanied by species-specific stereotypical productions of cells, commencing with an asymmetric cell division which produces a meristemoid having a prescribed number of future divisions and concludes with a symmetric division that produces a pair of guard-cells. Where all cells of the stomatal cellular complex descend from a meristemoid, and where subsidiary epidermal cells are produced from intervening steps, the pathway is said to be mesogenous. It is often found in dicot plants. In contrast, the perigenous pathway often consists of fewer divisions of the meristemoid and incorporates into the ontogeny of the stomatal complex one or more of the protodermal cells which neighbour the meristemoid; it is their asymmetric divisions which produce subsidiary cells. This pattern is often found in monocots. The auto-reproductive meristemoidal state may, in certain cases of the mesogenous pathway, be perpetuated by means of a stomatogenic branching process in one of the subsidiary cells, as shown by the formation of “satellite” stomatal cellular complexes on leaves of Arabidopsis thaliana. L-system algorithms are developed that prescribe not only the cell divisions and transformations but also the stomatogenic cellular patterning that occurs throughout the angiosperms. Mutations of the patterning process, and natural variations, such as stomatal clustering, are also discussed. All the division patterns (normal, mutant, and unusual) necessary for the structuring of leaf stomatal complexes, including examples of the so-called “one-cell rule” of stomatal spacing, can be modelled by an appropriate deterministic L-division system. Because the division systems can be analogised to states of the wall and peripheral cytoplasm that attract the attachment of new division walls, this cytological aspect of meristemoids would appear to deserve more attention. Gene regulation is an additional component of stomatal construction. Such processes help to initiate the cytological analogues that are reproduced by L-systems within a framework composed of hitherto uncommitted protodermal cells. Gene regulation also terminates the auto-reproductive property of the division system and leads to the differentiation of the cells which construct the stomatal complexes.

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Notes

  1. 1.

    It has been said that Aristid Lindenmayer was one day passing a lecture room in which a lecture about formal languages was taking place. The speaker mentioned L(G): “Algae!” was Lindenmayer’s immediate reaction. After this “eureka moment”, he started to investigate applications of language theory to developmental biology. Algae constituted the first example (from Rozenberg and Salomaa 1986, p. 383–384).

  2. 2.

    The “sides”, or “edges”, of a cell are those seen in two-dimensional plan view, as might be observed in a microscope. In their three-dimensional context, the “sides” are actually “side walls” or “wall facets”.

  3. 3.

    Meristemoids have been variously defined, but generally they are cells capable of renewed meristematic activity (of “reactivated embryonality”, as Bünning (1956, 1965) put it when he introduced the term “meristemoid”), which leads their descendents to a fate different from that of neighbouring cells. In Bünning’s writings (Bünning 1956, 1965), emphasis is placed on a hypothetical inhibitory field emanating from each meristemoid and which is believed to regulate the positioning of new meristemoids (see Sachs 1991); but this physiological aspect is supplementary to the more anatomically based definition provided here. Before a meristemoid is produced, there is a polarisation of cytoplasm in the mother cell; this cell subsequently divides asymmetrically to produce one meristemoid containing the dense polarised cytoplasm and another type of daughter cell (See also footnote 11).

  4. 4.

    All these mentioned studies of S and g cell properties were made on monocot species where the origin of the S cells is different to that of S cells in most dicots. Whether those cells of dicots which are believed to be S cells behave similarly to the S cells of monocots is a question that has been rather neglected by physiologists.

  5. 5.

    These divisions are often called “amplification” divisions. They are, however, more like a series of asymmetric stem-cell divisions than a series of true amplification, or proliferative, divisions which lead to an increase in the number of cells derived from a stem-cell. They have also been called “formative” divisions by Charlton (1990), a term which we, too, prefer.

  6. 6.

    Payne (1979) proposed the terms parameristic, diameristic and anomomeristic for where the respective angles of division of the guard cell, θg, were 0º, 90º and irregular (usually 120º). In certain cases, θg is regulated by the ability of the division apparatus of the guard mother cell to rotate during mitosis (Palevitz 1986), and this may follow as a consequence of the orientation of leaf surface growth (Lück and Lück 1961).

  7. 7.

    Agenous stomata have a long history, being found on the surfaces of fossil plants dating from the Silurian and Devonian era (Edwards et al. 1998), thereby pre-dating by millions of years the ancestors of modern plants. It can be speculated that they arose from protodermal cells which occasionally gave rise to guard mother cells, and that these cells, for some reason, failed to expand as much as their neighbouring cells. Maybe their small size was maintained by the development of a special type of cuticle on their external surface. But the small cells could still divide. When they did so, two guard cells were produced. Separation of the division wall between the two sister guard cells brought into being the stomatal pore, which overlies a substomatal chamber in the hypodermis, a chamber produced by a cell separation event that focusses upon the inextensible guard cells above.

  8. 8.

    Lateral root primordia are arranged with a definite spacing interval in longitudinal ranks along the parent root. The circumferential spacing of these primordia depends upon the distribution of vascular strands. If a root were rolled out flat, in two-dimensions, the distribution of its primordia would resemble that of the meristemoids upon the surface of a leaf.

  9. 9.

    The areole of the leaf is not to be confused with the quite different areole of cactus stems! The leaf areole domain referred to here has also been designated by the more cumbersome, but more exact, term “bundle sheath extension compartment” (Terashima 1992). “Stomatal complex domain” or “stomatal complex compartment” might be equally appropriate terms. The areole comes to develop as a packet of related cells which contains a generative cell (meristemoid) with regular cell productions, just as postulated for primitive apices (Barlow et al. 2000). Then, one set of cell walls (say, the oldest walls) bordering the areole cell-packet initiates vein formation. Vein formation itself can also be considered as a deterministic process (Lück and Lück 1981). In this respect, it could underpin some of the other, but equally hypothetical, chemical morphogen-based scenarios for leaf vein development. The formation of veins and areoles is also reminiscent of the cracking of surfaces due to their expansion or contraction (Iben and O’Brien 2009). Thus, veins might follow the path of intercellular ‘cracking’, or splitting, and the areas of tissue (especially epidermis) thus defined become areoles within which stomatal meristemoids form.

  10. 10.

    Despite extensive quantification of features of the leaf epidermis in relation to stomata (e.g. Tichá 1982), relatively little is known about the spatial disposition of cell types immediately below the epidermis and its structures.

  11. 11.

    It is remarkable that stomatal meristemoids have never been reported to produce directly a root or shoot apex; therefore, they do not seem to have the embryonic potentials suggested by Bünning (1956, 1965) (however, the property of “embryonality” – the term used by Bünning in the context of the meristemoid, appears to refer to the sites of synthesis of new cytoplasm in these cells, and even in the mother cell of the meristemoid). Leaf epidermal cells, and even guard cells, can be induced to divide (Tucker 1974), but they do so only within the confines of the leaf surface. Could it be that the tough, waxy surface of the leaf restricts meristemoid growth and division? But this is not to say that epidermal outgrowth can never occur: trichomes are one example where outgrowth does take place. Epiphylly is also well known in a few taxa. However, this last-mentioned process does not involve the stomatal meristemoids on the leaf surface but concerns mainly a sub-epidermal layer (see Brossard 1973). Yet, these sub-epidermal groups of cells do have “embryonality” since they are able to generate all the tissues of the new plantlet. They would also be meristemoids in Bünning’s sense.

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Authors and Affiliations

  1. Department of Biological Sciences, University of Bristol, Woodland Road, Bristol, BS8 1UG, UK

    Peter Barlow

  2. Chemin du Val d’Arenc 1226, Le Beausset, F 83330, France

    Jacqueline Lück

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  1. Peter Barlow
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  2. Jacqueline Lück
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Editors and Affiliations

  1. Inst. Botanik, TU Darmstadt, Schnittspahnstr. 3-5, Darmstadt, 64287, Germany

    Ulrich Lüttge

  2. Fakultät für Biologie, LS für Experimentelle Ökologie, Universität Bielefeld, Bielefeld, Germany

    Wolfram Beyschlag

  3. FB Biologie, Abt. Allgemeine Botanik, TU Kaiserslautern, Erwin-Schrödinger-Str., Kaiserslautern, 67663, Germany

    Burkhard Büdel

  4. Cardiff School of Biosciences, University of Cardiff, Cardiff, United Kingdom

    Dennis Francis

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Barlow, P., Lück, J. (2010). Transformations of Cellular Pattern: Progress in the Analysis of Stomatal Cellular Complexes Using L-Systems. In: Lüttge, U., Beyschlag, W., Büdel, B., Francis, D. (eds) Progress in Botany 71. Progress in Botany, vol 71. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-02167-1_3

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