The Formation of Catenate Foliar Gemmae and the Origin of Oil Bodies in the Liverwort Odontoschisma denudatum (Mart.) Dum. (Jungermanniales): a Light and Electron Microscope Study

Abstract

This article describes the ultrastructural events associated with the differentiation and liberation of the exogenous gemmae produced in branched acropetal chains along the margins of the leaves in the liverwort Odontoschisma denudatum. Formation of a dorsal protrusion from young leaf cells containing a large central nucleus, small vacuoles, starch-free chloroplasts, scattered cytoplasmic lipid droplets but no oil bodies, signals the onset of the formation of the initial cell of a gemmiferous filament. The protrusion enlarges and the nucleus migrates into its base, therein dividing with the equator of the spindle virtually filling the central isthmus between the leaf surface and the now swollen tip of the initial cell. Subsequent divisions of the initial cell produce a chain of cells in atropetal succession. Transversely orientated microtubules line the cortical cytoplasm along the lateral walls of the terminal cells of the gemmiferous filaments, but are absent from the tips, thus suggesting that these cells elongate by intercalary, rather than by tip, growth. During mitosis microtubules are closely associated with the envelopes of spindle-shaped prophase nuclei, radiate from ill-defined spindle poles surrounded by plastids at metaphase and anaphase and form a dense phragmoplast array during telophase. Pre-prophase bands are absent and it may be that the nuclear equator determines the plane of division in gemmiferous filaments. Chloroplast division, associated with extremely transient plastid-dividing rings, takes place during interphase. Lateral branches of the growing filaments arise from subapical cells by reiteration of the first division mechanism. Immediately following the proliferative divisions, which take place in cells measuring only 5-6 μm in diameter, oil bodies suddenly appear as flat pleomorphic cisternae associated with endoplasmic reticulum and occasional microtubules. Their contents are electron-transparent apart from scattered osmiophilic droplets. Throughout their ontogeny the oil bodies are closely associated with cytoplasmic lipid bodies but there is no evidence of fusion. The nascent oil bodies swell rapidly to their final diameter, become ovoid to spherical in outline and are eventually suspended by fine cytoplasmic bridges within the vacuoles. The latter rapidly increase in size together with an expansion of the cells themselves until these reach their final diameter and length. The final event in gemma maturation is an endogenous division with the formation of a new internal wall along a phragmosome. Separation of the bicellular gemmae proceeds basipetally and involves the appearance of an electron-transparent line along the middle lamella in the cross walls, which often develop convex thickenings, and severing of the plasmodesmata. After their liberation shallow scars are visible on the leaf surface under the SEM. Gemma maturation sees a marked increase in the electron-opacity of the walls and dense staining of these together with Golgi vesicles with the periodic acid/thiocarbohydrazide/silver proteinate test for non-cellulosic carbohydrates. This change in wall chemistry and ultrastructure may be related to the fact that the maturing gemmae become extremely water repellant and are probably dispersed either on the surface of water films or in the air.