Independence of Tissues Derived From Apical Layers in Ontogeny of the Tobacco Leaf and Ovary

Abstract

Six different homoplastidic periclinal chimeras of tobacco carrying the plastogene DP1 were selected after somatic segregation in heteroplastidic seedlings. Direct observation of the plane of division in epidermal cells of young leaves, and the number and size of sub‐epidermal green spots on leaves with the Green‐White‐White (G‐W‐W) pattern of variegation, indicated that the ratio of periclinal to anticlinal divisions in L‐I during development of the lamina was 1:3100. The number of green and white seedlings obtained from the different chimeral branches indicated a similar frequency of periclinal divisions in development of the ovary. The arrangement of green and white tissue in mature leaves of the various chimeral types indicated the extent of participation by the three apical layers in the initiation of the buttress, development of the axis, and formation of the lamina. During development of the lamina there must be three independent initial‐groups present. L‐I and L‐II initials remain marginal, but early in the growth of the lamina the leading edge of tissue derived from L‐III becomes separated from the submarginal (L‐II) initials by the products of frequent periclinal divisions of the L‐II initials.

Growth coordination and the shoot epidermis

“…Our knowledge of cell lineage organization and inter-cell-layer communication has been gained largely from studies using chimeric plants or genetic mosaics [2,4,5]. These studies rely on the ability to easily identify two groups of genetically distinct cells.…”

“…The L1 and L2 divide in a stereotypical manner, predominantly anticlinal to the plane, whereas the cells in the L3 undergo both anticlinal and periclinal divisions. Simply put, L1-derived cells form the epidermis and define the shoot/environment interface, the L2 gives rise to the photosynthesizing cells of the sub-epidermis, and L3-derived-cells comprise the ground tissues [2]. The extent to which each of these layers contribute to organ size and whether there is communication between these distinct cell layers has been a matter of interest for over a century; yet only recently have the molecular toolkits become available to address these questions in an intact, growing organism [3,4].…”

Shoot Meristem Formation in Vegetative Development.

“…As a result of their anticlinal divisions, cells within each of the tunica layers maintain a separate lineage from cells above and/or below them. The use of chimeric plants with one complete cell layer that is genetically distinct from adjacent layers (periclinal chimeras) has demonstrated that the layered cellular organization of the meristem tends to be maintained in the stem and lateral organs of the shoot, although invasion of cells from one layer into another occurs frequently (Dermen, 1953;Stewart and Burk, 1970;Stewart and Dermen, 1979). In general, the outermost layer, termed L1, gives rise to the epidermis, whereas the inner layers, L2 and L3, contribute to the central tissues of the leaf and stem.…”

“…In general, the outermost layer, termed L1, gives rise to the epidermis, whereas the inner layers, L2 and L3, contribute to the central tissues of the leaf and stem. Although the stratified appearance of the SAM allows reasonable predictions regarding the fate of a cell, the study of lineage relationships in plants has shown that position rather than lineage is the most important factor in determining cell fate (Dermen, 1953;Stewart and Burk, 1970;Stewart and Dermen, 1979;see Clark, 1997;Laux and Jürgens, 1997;Poethig, 1997;Schiefelbein et al, 1997, all in this issue).…”

Between the sheets: inter–cell–layer communication in plant development

“…The study of periclinal chimaeras, in which meristems comprise layers showing differing phenotypic traits or expressing different markers, has allowed the contributions of different meristematic cell layers to leaf and organ primordia to be studied (Satina & Blakeslee 1941;Stewart & Burk 1970;Tilney-Basset 1986;Jenik & Irish 2000). In combination with clonal analysis, such studies have also allowed the developmental behaviour of cells derived from different apical meristematic cell layers to be followed during the course of organ development (Poethig 1987).…”