Syncytial-Type Cell Plates: A Novel Kind of Cell Plate Involved in Endosperm Cellularization of Arabidopsis

Abstract

Cell wall formation in the syncytial endosperm of Arabidopsis was studied by using high-pressure-frozen/freeze-substituted developing seeds and immunocytochemical techniques. The endosperm cellularization process begins at the late globular embryo stage with the synchronous organization of small clusters of oppositely oriented microtubules ( ‫ف‬ 10 microtubules in each set) into phragmoplast-like structures termed mini-phragmoplasts between both sister and nonsister nuclei. These mini-phragmoplasts produce a novel kind of cell plate, the syncytial-type cell plate, from Golgiderived vesicles ‫ف‬ 63 nm in diameter, which fuse by way of hourglass-shaped intermediates into wide ( ‫ف‬ 45 nm in diameter) tubules. These wide tubules quickly become coated and surrounded by a ribosome-excluding matrix; as they grow, they branch and fuse with each other to form wide tubular networks. The mini-phragmoplasts formed between a given pair of nuclei produce aligned tubular networks that grow centrifugally until they merge into a coherent wide tubular network with the mini-phragmoplasts positioned along the network margins. The individual wide tubular networks expand laterally until they meet and eventually fuse with each other at the sites of the future cell corners. Transformation of the wide tubular networks into noncoated, thin ( ‫ف‬ 27 nm in diameter) tubular networks begins at multiple sites and coincides with the appearance of clathrin-coated budding structures. After fusion with the syncytial cell wall, the thin tubular networks are converted into fenestrated sheets and cell walls. Immunolabeling experiments show that the cell plates and cell walls of the endosperm differ from those of the embryo and maternal tissue in two features: their xyloglucans lack terminal fucose residues on the side chain, and callose persists in the cell walls after the cell plates fuse with the parental plasma membrane. The lack of terminal fucose residues on xyloglucans suggests that these cell wall matrix molecules serve both structural and storage functions. INTRODUCTIONIn higher plants, new cell walls are formed during cytokinesis by fusion of Golgi-derived vesicles into cell plates. The structure that gives rise to the cell plate is the phragmoplast, a complex arrangement of microtubules, microfilaments, Golgi-derived vesicles, and endoplasmic reticulum that assembles during late anaphase and is dismantled once the new wall is complete (Staehelin and Hepler, 1996;Smith, 1999). The phragmoplast cytoskeleton consists of two oppositely oriented sets of microtubules with their plus ends in the plane of the cell plate and two corresponding sets of actin microfilaments that do not overlap or directly abut. The first phragmoplast microtubules appear to arise from remnants of the mitotic spindle, but all later ones are polymerized anew, forming a cylinder that consolidates by shortening in length and widening in girth. During cell plate expansion, the microtubules depolymerize in the center and repolymerize along the edge, transforming the phragm...

Electron tomographic analysis of post-meiotic cytokinesis during pollen development in Arabidopsis thaliana

“…In addition, we document the presence of molecules that link vesicles and membranous tubules during cell plate formation and the delivery of the ribosome-excluding cell plate assembly matrix to the division plane together with the vesicles. This report, together with recent studies on high-pressure-frozen/ freeze-substituted endosperm samples (Otegui and Staehelin 2000b;Otegui et al 2001), demonstrates that in different tissues of higher-plant cells cytokinesis can proceed by formation of different types of cell plate but never involves cleavage furrows.…”

“…A cell plate assembly matrix that excludes ribosomes is delivered to the division plane together with the first vesicles Previously, we have shown that a dense, ribosomeexcluding matrix surrounds the early membrane intermediates of developing syncytial-type cell plates (Otegui and Staehelin 2000b;Otegui et al 2001). We have also detected a similar matrix encompassing all the assembly intermediates during post-meiotic cell plates (Figs.…”

“…2, 3). Because these MT clusters resemble those involved in syncytialtype cell plate assembly in the endosperm (Otegui and Staehelin 2000b), we have also named them miniphragmoplasts. However, unlike those of the endosperm cells, the mini-phragmoplasts in microsporocytes form simultaneously across the entire division plane, and not only in the central region (Figs.…”

“…For most syncytial systems at least two different models of cell wall formation have been reported, either by cell plate assembly or by cleavage furrows (reviewed in Otegui and Staehelin 2000a). We have recently solved the controversy surrounding the process of endosperm cellularization in Arabidopsis by studying cells preserved by high-pressure freezing/freezesubstitution techniques (Otegui and Staehelin 2000b;Otegui et al 2001). These studies provided unambiguous proof for the involvement of cell plates in endosperm wall formation.…”

Cell Wall Polysaccharide Synthesis

“…In most monocots XG contains less xylose and galactose and does not contain terminal fucose. The structure and molecular distribution of the side chains varies in different plant tissues and species (100)(101)(102).…”