Plant Nuclei Can Contain Extensive Grooves and Invaginations [W]

Abstract

Plant cells can exhibit highly complex nuclear organization. Through dye-labeling experiments in untransformed onion epidermal and tobacco culture cells and through the expression of green fluorescent protein targeted to either the nucleus or the lumen of the endoplasmic reticulum/nuclear envelope in these cells, we have visualized deep grooves and invaginations into the large nuclei of these cells. In onion, these structures, which are similar to invaginations seen in some animal cells, form tubular or planelike infoldings of the nuclear envelope. Both grooves and invaginations are stable structures, and both have cytoplasmic cores containing actin bundles that can support cytoplasmic streaming. In dividing tobacco cells, invaginations seem to form during cell division, possibly from strands of the endoplasmic reticulum trapped in the reforming nucleus. The substantial increase in nuclear surface area resulting from these grooves and invaginations, their apparent preference for association with nucleoli, and the presence in them of actin bundles that support vesicle motility suggest that the structures might function both in mRNA export from the nucleus and in protein import from the cytoplasm to the nucleus. INTRODUCTIONAlthough cellular function often requires maximization of surface area relative to volume, notably in organelles such as the endoplasmic reticulum (ER) and Golgi apparatus, traditional representations of the nucleus depict a rounded structure with little internal organization. Recently, however, the nuclei of animal cells have been found to show considerable spatial and structural organization at the chromosomal level. The discrete and comparatively stable territories that chromosomes occupy within the nucleus are separated by interchromosomal domains through which transcribed RNA and other macromolecules can diffuse (reviewed in Lamond and Earnshaw, 1998). Animal nuclei also sometimes deviate from the characteristic rounded shape. Deviations include a folded, grooved, or notched surface (Majno et al., 1969) and tubular invaginations. Electron microscopy has shown that these nuclear invaginations can penetrate deep into the nucleus and confirmed the presence of the double membrane of the nuclear envelope (Ellenberg et al., 1997;Fricker et al., 1997;Clubb and Locke, 1998). However, revelation of the full nature of nuclear invaginations in living animal cells has required confocal microscopy of fluorescent dyes (Fricker et al., 1997;Lui et al., 1998aLui et al., , 1998b or green fluorescent protein (GFP) fusion proteins targeted to the nuclear envelope (Ellenberg et al., 1997;Broers et al., 1999). The number and nature of invaginations vary from cell type to cell type, ranging from simple invaginations to intricate branched structures that can penetrate into and through the nucleus. Invaginations often associate with nucleoli (Fricker et al., 1997) and appear to be stable (Ellenberg et al., 1997;Broers et al., 1999). Nuclear grooves and invaginations substantially increase the surface area of the ...

Nuclear import and export of proteins in plants: a tool for the regulation of signalling

“…The depletion of transport factors in the animal in vitro import systems during permeabilisation has allowed biochemical approaches and greatly enhanced the characterisation of essential transport factors (GoÈ rlich et al 1994). However, a recent report demonstrated beautifully that plant nuclei can contain extensive grooves and invaginations (Collings et al 2000). This ®nding may provide a possible explanation of why nuclear transport factors are eectively trapped during the preparation of in vitro nuclear import systems.…”

Plastids and stromules interact with the nucleus and cell membrane in vascular plants

“…4a). These infoldings of the nuclear envelope are contiguous with the cytoplasm and have been shown to contain actin microfilaments (Collings et al 2000). Plastids were often observed within these channels and grooves (Fig.…”

“…In this report, we present evidence from Nicotiana tabacum (tobacco) and Arabidopsis thaliana (Arabidopsis) that many cell types exhibit interactions between plastids and nuclei. In some cases, we have observed plastids and stromules in nuclear grooves and invaginations (Collings et al 2000). Stromules also appear to join perinuclear plastids to the cell membrane in certain cell types.…”

The plant nuclear envelope

“…Although nuclei are typically depicted as spheres, the shape of the nuclear envelope can diverge greatly from this image. Significant grooves and invaginations, both static and dynamic in nature, have been found in both animal and plant nuclei [6,7]. These structural features increase the interaction surface between the nucleus and cytoplasm, and suggest that nuclear and cytoplasmic activities may be more structurally linked than was previously anticipated.…”