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植物细胞核的结构功能规律

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植物细胞核的结构功能规律植物细胞核的结构功能规律 The nuclear envelope in the plant cell cycle: structure, function and regulation 1. D. E. Evans, 2. M. Shvedunova and *3. K. Graumann + Author Affiliations 1. School of Life Sciences, Oxford Brookes University, Oxford OX3 0BP, UK *1. For corresp...
植物细胞核的结构功能规律
植物细胞核的结构功能规律 The nuclear envelope in the plant cell cycle: structure, function and regulation 1. D. E. Evans, 2. M. Shvedunova and *3. K. Graumann + Author Affiliations 1. School of Life Sciences, Oxford Brookes University, Oxford OX3 0BP, UK *1. For correspondence: kgraumann@brookes.ac.uk , Received July 15, 2010. , Revision received November 30, 2010. , Accepted December 3, 2010. Next Section Abstract Background Higher plants are, like animals, organisms in which successful completion of the cell cycle requires the breakdown and reformation of the nuclear envelope in a highly controlled manner. Interestingly, however, while the structures and processes appear similar, there are remarkable differences in protein composition and function between plants and animals. Scope Recent characterization of integral and associated components of the plant nuclear envelope has been instrumental in understanding its functions and behaviour. It is clear that protein interactions at the nuclear envelope are central to many processes in interphase and dividing cells and that the nuclear envelope has a key role in structural and regulatory events. Conclusion Dissecting the mechanisms of nuclear envelope breakdown and reformation in plants is necessary before a better understanding of the functions of nuclear envelope components during the cell cycle can be gained. Key words , Nuclear envelope , mitosis , cytokinesis , LINC complex , SUN domain proteins , nuclear envelope breakdown , nuclear pore complex , cell division , higher plant Previous SectionNext Section INTRODUCTION Higher plants, together with metazoans, undergo an open cell division. In contrast to lower eukaryotes including yeast and fungi, the nuclear envelope breaks down, exposing the chromosomes fully to the mitotic apparatus. This means that higher plants are complex organisms in which successful completion of the cell cycle requires first the breakdown and then the reformation of the nuclear envelope in a highly controlled manner. Interestingly, however, while the structures and processes show homology between plants and animals, there are remarkable differences in protein composition and function. This review will first introduce key elements of the composition of the nuclear envelope followed by an overview of the processes involving the nuclear envelope that govern progression through mitosis and cytokinesis. Previous SectionNext Section THE NUCLEAR ENVELOPE AS A SCAFFOLD-SUPPORTED STRUCTURE A key feature of the nuclear envelope, with significance for its breakdown and reformation, is its very close association with structural proteins both within and external to the nucleus. Rather than forming a pleomorphic ‘bag’ (albeit with perforations) surrounding the nuclear contents, the nuclear envelope in an interphase cell is anchored internally to the scaffold of the nucleoskeleton and chromatin and externally to the cytoskeleton. In addition, proteins within the membrane are structurally associated with one another. The nuclear pores and proteins of the inner nuclear membrane (INM) interact with each other and with the nucleoskeleton while protein bridges span the perinuclear space linking proteins of the INM with proteins in the outer nuclear membrane (ONM), which in turn bridge to the cytoskeleton (Fig. 1; Gruenbaum et al., 2005; Starr, 2009). These interactions are important in positioning the structure and in maintaining its order; they must therefore be lost and reformed as the cell progresses through the cell cycle. Only recently has progress been made in identifying structural proteins of the nuclear envelope in plants (Meier and Brkljacic, 2009a; Graumann and Evans, 2010a; Graumann et al., 2010) and has exploration of their interactions begun. View larger version: , In this page , In a new window , Download as PowerPoint Slide Fig. 1. Scaffold-structures support the nuclear envelope. In both animals and plants, the nuclear envelope is associated with nucleoskeletal and cytoskeletal structures. In animals the lamina is connected to the inner nuclear membrane by membrane-intrinsic proteins such as LBR, Man1, SUN domain proteins and Laps, which also associate with chromatin. KASH-domain proteins such as nesprins bind to SUN domain proteins and stretch into the cytoplasm to link to cytoskeletal elements such as actin and microtubule organizing centres (MTOC). In plants, a lamina-like network is also present and is hypothesized to consist of filamentous proteins such as NMCP1/2 and LINC1/2. How these proteins and the meshwork are associated with the nuclear envelope remains to be established but AtSUN1 and AtSUN2 are putative anchor candidates. Cytoskeletal structures such as actin and gamma tubulin ring complexes (γ-TURC) are associated with the cytoplasmic face of the plant nuclear envelope but similarly their anchoring mechanisms remain unknown. The nuclear lamina Immediately beneath the nuclear envelope of animal cells lies a meshwork of proteins known as the lamina (Fig. 1; Gruenbaum et al., 2005). It is made up of type-5 intermediate filament proteins known as lamins together with a number of additional components to which nuclear envelope, nuclear pores and chromatin are attached by protein interactions (reviewed in Wilson and Berk, 2010). The lamina is attached to the INM by interactions with membrane integral proteins, which include lamina-associated polypeptides; the lamin B receptor (LBR), a multipass membrane protein; members of the LEM (LAP2, emerin, Man1) domain family and the Sad1/UNC84 (SUN) domain proteins (Gruenbaum et al., 2005; Wilson and Berk, 2010). Thus the interphase nuclear envelope is closely and multiply associated with the lamina and with chromatin in animal cells (Fig. 1). Sequence homologues of the lamins and of many of the proteins involved in anchoring the mammalian lamina and chromatin to the nuclear envelope are absent in plants and fungi (reviewed in Brandizzi et al., 2004, Meier, 2007; Graumann and Evans, 2010a). However, evidence for a lamina-like structure has been increasing. This includes electron microscopy, where a protein meshwork is apparent adjacent to the nuclear envelope interconnecting the nuclear pores (Fiserova et al., 2009), immunological identification of nuclear intermediate filament-like proteins (Minguez and Diaz de la Espina, 1993; Masuda et al., 1997) and the presence of plant-specific filamentous proteins at the nuclear periphery (Masuda et al., 1997; Gindullis et al., 2002; Dittmer et al., 2007). These include Daucus carota nuclear matrix constituent protein (NMCP) 1 and NMCP2 and their Arabidopsis thaliana homologues little nuclei, LINC1 and LINC2 (Fig. 1; Masuda et al., 1997; Dittmer et al., 2007). While no direct evidence for their presence in the lamina-like meshwork exists so far, it is hypothesized that they fulfil similar functions to lamins in plants. Evidence for this comes from studies of AtLINC1 and AtLINC2 mutants, which have smaller nuclei and altered nuclear morphology (Dittmer et al., 2007). How these proteins retain their localization at the nuclear periphery and what interaction networks they are involved in remains to be elucidated (Fig. 1). SUN domain proteins and the linker of nucleoskeleton and cytoskeleton (LINC) complex The SUN domain family has been shown to be ubiquitously present in higher and lower eukaryotes (reviewed in Starr, 2009; Graumann et al., 2010) and provides protein interactions both within and between nuclear envelope proteins and the nucleoskeleton (Fig. 1). The SUN domain proteins are type-2 membrane proteins of the INM and interact with proteins of the Klarsicht/Anc-1/Syne-1 homology (KASH) domain family of ONM proteins, with the SUN and KASH domains interacting in the periplasmic space separating the two membranes (Fig 1; reviewed in Worman and Gunderson, 2006; Starr, 2009). This bridge, known as the LINC (linker of nucleoskeleton and cytoskeleton) complex (Crisp et al., 2006) is multifunctional with a variety of SUN and KASH domain proteins facilitating interactions with a wide range of cytoskeletal and nuclear elements. SUN domain proteins are present in organisms undergoing both open and closed division. In yeast, SUN domain proteins Sad1 (Schizosaccharomyces pombe) and Mps3 (Saccharomyces cerevisiae) are located at spindle pole bodies (SPBs) and the nuclear envelope (Tran et al., 2001; Bupp et al., 2007). The SPB is a multilayered structure closely associated with the nuclear envelope and contains a central plaque associated with a region of the nuclear envelope, the half bridge, to which SpSad1 and ScMps3 are localized (Hagan and Yanagida, 1997; Jaspersen et al., 2006). Putative homologues of SpSad1 were identified in arabidopsis (Van Damme et al., 2004) and Oryza sativa (Moriguchi et al., 2005) with location to the phragmoplast and mitotic spindle observed in the former study. Recently, they have been characterized in detail as classical SUN domain proteins in the authors’ laboratory; AtSUN1 and AtSUN2 localize to the nuclear envelope in interphase and show the characteristic domain structure of the family (Graumann et al., 2010). While their protein binding partners have yet to be identified, they provide first evidence of a putative LINC complex in plants (Fig. 1). The nuclear pore complex Nuclear pore complexes (NPCs) are large protein assemblies structurally conserved in animals, plants and fungi regardless of whether they show open or closed mitosis (Mans et al., 2004; Lim et al., 2008). They are composed of multiple copies of approx. 30 different proteins, termed nucleoporins (Nups) (Margalit et al., 2005). These include soluble proteins and integral membrane proteins (Cohen et al., 2005), which are inserted into the pore membrane – a domain of the nuclear envelope that provides the only connection between INM and ONM. Many nucleoporins group together to form subcomplexes. The fully assembled NPC has a total mass of approx. 120 MDa in vertebrates and 60 MDa in yeast (Harel et al., 2003). Plant NPCs are intermediate in size (approx. 105 nm) between yeast (approx. 95 nm) and Xenopus laevis (approx. 110–120 nm) (Fiserova et al., 2009). NPCs posses octagonal symmetry around the axis of transport (D'Angelo and Hetzer, 2008). They mediate both passive diffusion and active nucleocytoplasmic transport. Typically, proteins and mRNAs require targeting motifs – nuclear localization signals for import and nuclear export signals for export – which are recognized by karyopherins, transport proteins that mediate the traffic of the cargo molecule through the pore (Lusk et al., 2007). A third of nucleoporins carry phenylalanine–glycine (FG) repeats, which face the inside of the pore and associate with the karyopherins to direct their passage (Cronshaw et al., 2002). In animal cells, filamentous proteins extend into the cytoplasm and form a structure resembling a basket on the nucleoplasmic face. Cytoplasmic filaments are not always present in micrographs of plant NPCs, although a ‘basket’ structure of filaments is present extending into the nucleoplasm (Fiserova et al., 2009). The whole structure is arranged around the membrane intrinsic proteins of the pore membrane. Of three such proteins identified, Pom121 is only found in vertebrates (Mans et al., 2004); Ndc1 has been shown to be essential for NPC assembly in mammals and yeast (Mans et al., 2004; Cohen et al., 2005; Stavru et al., 2006a). Gp210, a single pass membrane glycoprotein has also been identified in plants (Cohen et al., 2005), together with a homologue of Ndc1 (Stavru et al., 2006b). Of the 30 or so soluble nucleoporins present in animal and yeast, only seven homologues have been identified in plants so far. They include arabidopsis Nup160, Nup96, Nup88 and Tpr/NUA as well as Nicotiana bethamiana Rae1 and Lotus japonicus Nup133 and Nup85 (Xu and Meier, 2008; Meier and Brkljacic, 2009b). In addition, plant-specific NPC-associated proteins have been identified in arabidopsis. Tryptophan–proline–proline (WPP)-interacting proteins (WIPs) and WPP-interacting tail-anchored proteins (WITs) are thought to be localized in the ONM and pore membrane and are required for RanGAP anchorage (Xu et al., 2007a; Zhao et al., 2008; Meier and Brkljacic, 2009a). Previous SectionNext Section THE NUCLEAR ENVELOPE IN THE CELL CYCLE Duplication of the NPC precedes nuclear envelope breakdown (NEBD) The first major change in structure of the nuclear envelope in higher plants and metazoans occurs in G, prior to NEBD, when replication of 2 the NPCs occurs, accompanied by enlargement of the nuclear envelope and duplication of the DNA (Tran and Wente, 2006; Fiserova et al., 2009). The mechanism for the insertion of the NPCs is still a subject of debate; it either requires joining of the INM and ONM to create a pore into which the NPC proteins insert (a process that requires protein interaction with the membrane) or nucleoporins are inserted and cause fusion of the ONM and INM, after which recruitment of the other nucleoporins follows (Tran and Wente, 2006; reviewed in Hetzer, 2010). Membrane fusion must occur at the luminal face of the membranes to establish the pore and must therefore be a process different from that of the secretory pathway, where fusion is from the opposite side of the membrane. Proteins are then added from both the nucleoplasmic and cytoplasmic face (D'Angelo et al., 2006). The mechanism for the formation of the pore by joining the INM and ONM to create the pore membrane remains unknown. However, Drin et al. (2007) have shown that Nup133 contains an alpha helical domain that senses membrane curvature. If sensing curvature by this domain is a prerequisite for the addition of the other nucleoporins, it implies that membrane fusion and pore formation precede the construction of the NPCs (Hetzer, 2010). Studies have concentrated on the second time NPCs are formed, reassembling during nuclear envelope reformation, and will therefore be described later in this review. It is interesting to note that at this stage, as insertion of NPCs has preceded NEBD, the processes parallel those in eukaryotes with a closed cell division. In yeast, which shows closed division, the process of inserting nuclear pores has been characterized in detail, with the pore domain transmembrane proteins (Pom34, Pom152 and Ndc1) marking the point of insertion of the NPC, possibly by bringing ONM and INM together. Nuclear pore assembly involves Nups59/53, integral membrane proteins Pom34 and Pom152, to which Nup170 and membrane-integral nucleoporin Ndc1 attach (Onischenko et al., 2009). The importance of Nup170 is indicated by the fact that when it, and its homologue Nup157, are depleted, pores form but are mis-located to the INM and cytoplasm rather than creating true pores (Dawson et al., 2009). The insertion of NPCs into the plant nuclear envelope in interphase has received little attention. In a recent study, Fiserova et al. (2009) observed plant NPCs in 3-d- and 10-d-old tobacco BY-2 suspension ?2cultures. The NPCs were highly abundant in all cells (40–50 µm). The authors suggest that a significant proportion of the 3-d-old cells were likely to be in S phase. At this stage, NPCs were distributed over the nuclear surface, with around 30 % of pores in connected pairs. Pores in 3-d-old cells appeared simpler than those in older cells, and the cytoplasmic ring thinner, with structures similar to those observed in xenopus oocytes. However, to date, antibody and molecular probes have not been available to permit detailed sequential analysis of NPC formation in plants and the hypothesis that the processes involved are the same as those in animals or yeast has yet to be tested. Plants possess a fully functional Ran cycle, involved in directing traffic through the pores, although the Ran nucleotide exchange factor, regulator of chromatin condensation 1 (RCC1) has not yet been identified, and RanGAP is attached to the NPCs by interaction via an N-terminal WPP domain with a novel plant family of nucleoporins termed WIPs and WITs (Rose and Meier, 2001; Jeong et al., 2005; Xu et al., 2007a; Zhao et al., 2008) rather than by sumoylation (as in animal cells; Meier, 2007). In addition to this role, Ran is also directly involved in pore assembly. In yeast, high levels of Ran-GTP and decreased importin β stimulate pore formation (Harel et al., 2003; Walther et al., 2003a, b). In xenopus oocytes, the nuclear envelope with nuclear pores assembles around beads coated with the Ran, forming transport-competent pseudo-nuclei in a process stimulated by RCC1 (Zhang and Clarke, 2000). Recently, importin β has also been shown to be essential to the process by which nuclear pore assembly is initiated on chromatin (Rotem et al., 2009). Nuclear envelope breakdown: loss of NPCs and selective permeability The breakdown of the nuclear envelope and its interaction with the endoplasmic reticulum (ER) is central to the cell division process in all organisms undergoing an open division. In animals, the nuclear envelope in interphase G is closely associated with tubular ER; thus 2 membrane intrinsic proteins can migrate readily into the ER network, which will constitute the ‘mitotic ER’ or ‘mitotic membranes’. Prior to the release of these proteins from the structural interactions that retain them at the nuclear envelope, the NPCs must be removed, providing free permeability between nucleoplasm and cytoplasm. Pore removal is a highly regulated process with the soluble NPC components migrating to the cytoplasm or becoming part of the mitotic apparatus, some remaining as protein complexes (reviewed in Hetzer, 2010). Breakdown of the NPCs occurs rapidly. Initially, Nup98 is removed (Griffis et al., 2002), followed by loss of the other nucleoporins (Dultz et al., 2008). In animal cells, NEBD occurs in prometaphase while in plants it is slightly earlier in late prophase (Rose, 2007). A strong structural link between proteins of the NPC and the nuclear lamina is indicated for animals; mutation, down-regulation of expression, or introduction of Fab fragments of antibodies to gp210 in Caenorhabditis elegans results in failure of the lamin nucleoskeleton to depolymerize. This results in a ‘twinned nucleus’ phenotype. Phosphorylation of the C-terminus of gp210 by cyclin B is essential for NEBD (Galy et al., 2008). Understanding of the processes involved in the loss of NPCs in plants is limited; only recently has progress been made in identifying plant nucleoporins and the necessary tools are only now becoming available to localize NPCs in mitotic structures or to follow their removal from the membrane. So far, the mitotic localization of only two plant nucleoporins is known: (1) arabidopsis NUA/Tpr, which is associated with the nuclear pore basket, migrates to the mitotic spindle in prometaphase (Xu et al., 2007b); and (2) tobacco Rae1 which associates with mitotic microtubules including the pre-prophase band (PPB), spindle and phragmoplast and appears to be required for mitotic events (Lee et al., 2009). Deletion or down-regulation of the gene causes defects in the spindle organization, chromatin alignment and segregation as well as decreased levels of cyclin B, cyclin-dependent kinase B1-1 (CDKB1-1) and histones H3 and H4 (Lee et al., 2009). Nuclear envelope breakdown: loss of structural interactions As already described, the structure of the nuclear envelope is maintained by a variety of interactions between the proteins of the envelope and nuclear pores and with associated proteins of the nucleoskeleton and cytoskeleton. These structural interactions must be broken down before the nuclear envelope components can migrate into the membranes of the mitotic apparatus or to create the structures of the mitotic apparatus. The removal of NPCs has a number of consequences, including the loss of the pore-dependent selective permeability of the membrane. Exposure of the nucleoplasm to cytoplasm permits a cascade of phosphorylation events. Entry of cyclin-dependent kinases (CDKs) and cyclin B1 results in dissociation of proteins of the lamina and INM, which are then released into the ER membranes. As maintenance of much of the structure of the nuclear envelope is dependent on physical associations of this nature, breakdown then progresses rapidly with nuclear-envelope components now free to migrate to the mitotic ER. Dephosphorylation at the end of division allows these interactions to be established again aiding in the reformation of the nuclear envelope (Anderson and Hetzer, 2008; reviewed in Guttinger et al., 2009). Progress through NEBD is regulated by aurora kinases and CDKs. How these kinases regulate plant NEBD and reformation remains to be established; however, aurora kinases are associated with the plant nuclear envelope in interphase and localize to the mitotic spindle, centromeres and phragmoplast in division. They phosphorylate histone H3 and are involved in chromosome segregation and cytokinesis (Demidov et al., 2005; Kawabe et al., 2005). Plant B1 cyclins have been found to accumulate at the nuclear envelope (Rose et al., 2004). The down-regulation of cyclin B and CDKB1-1 in combination with decreased mitotic activity in NbRae1 mutants suggests their involvement in plant mitosis progression (Lee et al., 2009). In addition to kinases, RanGAP plays a critical role in NEBD (Meier and Brkljacic, 2009b). As well as localizing to the nuclear envelope, arabidopsis RanGAP labels the PPB and the cortical division zone and is involved in maintaining the division plane and cell file organization in root tip cells. Depletion of the protein arrests dividing cells in metaphase/anaphase and results in cell death in the root tip meristem (Xu and Meier, 2008; Meier and Brkljacic, 2009b). Physical forces are also involved in NEBD as microtubule–dynein interactions are believed to draw the membrane away from the lamina (Beaudouin et al., 2002; Salina et al., 2002; Muhlhausser and Kutay, 2007; Stewart et al., 2007), although Lenart et al. (2003) suggest that NEBD can occur in the absence of a microtubule motor. The process in plants is complicated by consequences of the need to establish a precise plane of division in a walled structure. Here, the PPB of microtubules predicts the division plane. Tearing of the nuclear envelope occurs where ONM and PPB are closest to one another and before the PPB disintegrates (Dixit and Cyr, 2002; Brandizzi et al., 2004, Rose et al., 2004; Evans et al., 2009). Protein components of the nuclear envelope, once released from the associations, are relocated to the mitotic membranes in both animals (Andeson and Hetzer, 2008) and plants (Irons et al., 2003; Brandizzi et al., 2004; Evans et al., 2009). When mammalian LBR–GFP is expressed in plants, it is localized to the nuclear envelope in interphase and distributes throughout the mitotic membranes following NEBD (Fig. 2; Irons et al., 2003; K. Graumann, unpubl. res.); this is also true of the two arabidopsis SUN domain proteins AtSUN1 and AtSUN2 (Van Damme et al., 2004). In contrast, an 2+immunocytochemical study of the tomato Ca pump LCA, suggested specific localization to regions of spindle membranes, possibly related 2+to its function in regulating Ca signalling in mitotic events (Downie et al., 1998; Brandizzi et al., 2004). View larger version: , In this page , In a new window , Download as PowerPoint Slide Fig. 2. Nuclear envelope membranes in cell division. (A) In BY-2 cells stably expressing LBR–GFP (green) and H2B-CFP (magenta) the nuclear envelope marker is present at the nuclear periphery in interphase. As the nuclear envelope breaks down, the protein disperses into the ER and mitotic membranes associated with the spindle. In late anaphase, LBR–GFP locates to the reforming nuclear envelope and is present in the phragmoplast (through to cytokinesis). (B) Model for the presence of nuclear envelope membranes in cell division. From studies with LBR–GFP and other nuclear envelope-associated proteins such as the SUNs, WIPs and WITs, it is suggested that after NEBD, nuclear envelope proteins migrate to the mitotic ER membranes and re-emerge during nuclear envelope reformation. In addition, most of them also localize to the cell plate indicating a structural and functional link between these two membrane systems. During NEBD, the lamina-like meshwork underlying the INM also disintegrates. Two putative constituents of the plant lamina are Apium graveolus NMCP1 and NMCP2 (Kimura et al., 2010). The two proteins are present at the nuclear periphery in interphase but lose their associations with the nuclear envelope during prometaphase. While AgNMCP1 disperses throughout the spindle and reassembles around the decondensing chromatin in late anaphase, AgNMCP2 locates to the cytoplasm in vesicular structures and is recruited to the chromatin in telophase. This suggests a sequential assembly of the plant lamina (Kimura et al., 2010). Previous SectionNext Section BEHAVIOUR OF THE MITOTIC MEMBRANES AND REFORMATION OF THE NUCLEAR ENVELOPE NEBD in plants is accompanied by the formation of the structures of the plant mitotic apparatus with cisternal sheets of mitotic membranes located at the poles and tubular membranes running into , 2004). the mid-zone (Fig. 2; Hawes et al., 1981; Van Damme et al. These structures are dynamic and may be involved in ionic signalling and regulation of the division process. They remain until late anaphase, when the reformation of the envelope commences in both plants and animals (Fig. 2). Formation of the new nuclear envelope requires the dynamic change of tubular ER membrane into the flat sheets that will ultimately form a new envelope. Studies in animal cells show that this involves the fusion of the ends of ER tubules with chromatin. Several nuclear envelope-intrinsic proteins, including LBR, Lap2β and the SUN domain protein SUN1, have been shown to bind to chromatin (Collas et al., 1996; Pyrpasopoulou et al., 1996). A significant role for mammalian SUN1 in nuclear envelope reformation is suggested; it is present in membrane tubules in anaphase; interacts with histone acetyltransferase resulting in further chromatin decondensation and its deletion results in delayed formation of the new nuclear envelope (Chi et al., 2007). It has yet to be established whether plant SUN domain proteins fulfil a similar role. Following binding, flattening of the membranes is mediated by reticulons; reticulon 4A is required for nuclear envelope expansion (Kiseleva et al., 2007). Conservation of mechanisms between plants and animals is suggested by experiments showing that complete nuclear envelopes and NPCs reform when plant cell extract is incubated with animal DNA and vice versa (Rose et al., 2004). Demonstration of the presence of a fluorescent construct of AtSUN1-YFP in the mitotic membranes of higher plants suggests that it has an equally important role in plant nuclear envelope reformation to that in animals (K. Graumann, unpubl. res.). Plant reticulon homologues have also been identified (Nziengui et al., 2007; Tolley et al., 2008; Sparkes et al., 2009), in some cases associated with the nuclear membranes (Sparkes et al., 2010). Reformation of NPCs The next stage of the process involves the reformation of the NPCs; the second time NPCs have been added to the nuclear envelope in the cell cycle. Evidence for the order of events is largely derived from mammalian cultured cells or xenopus egg extracts (Bodoor et al., 1999; Dultz et al., 2008). The first events occur when members of the Nup107–160 complex bind to chromatin in early anaphase. This event is mediated by a large protein, Elys (Rasala et al., 2006; Franz et al., 2007; Gillespie et al., 2007). Elys contains an AT-hook DNA-binding motif and acts as an adaptor. In xenopus oocytes, Elys will recruit Nup107–160 in the absence of a membrane (Rasala et al., 2008) and involves importin β (Rotem et al., 2009). Association of Nup153 and Nup50 occurs shortly after the metaphase–anaphase transition (Dultz , 2008), forming a ‘prepore’ on the chromatin. Addition of et al. Pom121 in early anaphase results in fusion of the prepore with the nascent nuclear envelope (Bodoor et al., 1999; Daigle et al., 2001). The next nucleoporin to bind is Nup98, then Nup62 and Nup93 subcomplexes are recruited. An NPC containing these is transport competent in the presence of importin α (Dultz et al., 2008). The Nup62 and Nup93 complexes, Nup359, and Nup214 associate with the pore in telophase. The remaining components of the NPC, Tpr and gp210, assemble in early G phase of the cell cycle (Dultz et al., 2008). 1 As considered above in interphase, the absence of appropriate markers has prevented detailed description of the processes involved in the insertion of NPCs in telophase in plants. Previous SectionNext Section NUCLEAR ENVELOPE AND PHRAGMOPLAST: CONCLUDING THE DIVISION PROCESS The final process in the production of two daughter cells, accompanying the completion of the formation of the nuclear envelopes, is the formation of the new dividing cell wall. This is generated along the plane predicted by the PPB microtubules and involves considerable secretory vesicle activity. Use of the mammalian-based LBR–GFP expressed in plants shows that it is not only present in the newly forming nuclear envelopes, but also in the phragmoplast (Fig. 2; Irons et al., 2003; Brandizzi et al., 2004; K. Graumann, unpubl. res.). Other known nuclear envelope proteins, including the WIPs and WITs (other than WIP3; Zhao et al., 2008) and the SUN domain proteins AtSUN1 and AtSUN2 (K. Graumann unpubl. res.) are also observed in the phragmoplast. This may be due to lack of an effective sorting and retrieval mechanism due to the very high volume of membrane traffic directed to the cell plate; or may suggest a role for these proteins in cell wall formation. Interestingly, RanGAP1 is specifically localized to the position of the PPB and remains in location throughout division during mitosis and cytokinesis (Xu et al., 2007b). This suggests that a Ran gradient is formed that directs the vesicle traffic to the phragmoplast. As Ran has also been shown to be involved in the formation of the nuclear envelope and insertion of NPCs, it seems possible that similar mechanisms are involved in both systems resulting in nuclear envelope-directed vesicles trafficking to the phragmoplast and vice versa. Alternatively, some nuclear envelope proteins may be caught up in the rapid flow of membrane to the phragmoplast and are subsequently removed by recovery mechanisms. Previous SectionNext Section NUCLEAR ENVELOPE PROTEINS IN MEIOSIS In addition to NEBD and reformation, the nuclear envelope has a specific function in prophase 1 of meiosis – the anchorage of telomeres. In animal, yeast and some plants a chromosome bouquet is formed and anchored to the nuclear envelope via the telomeres. In animals and yeast this is essential for homologous pairing (reviewed in Tomita and Cooper, 2006; Roberts et al., 2009). In some plant species, however, this structure is not well defined. For instance, in arabidopsis, the telomeres are first clustered around the nucleolus and then move to the nuclear periphery (Roberts et al., 2009). Anchorage of the telomeres is mediated by the SUN domain components of the LINC complex in animal and yeast systems and deletion of these can result in abolishment of gametogenesis (Tomita and Cooper, 2006; Ding et al., 2007). How telomeres are linked to the nuclear periphery in plants remains to be investigated but the presence of plant SUN domain proteins suggests that similar mechanisms exist (Graumann and Evans, 2010b). Previous SectionNext Section CONCLUSIONS While the overall processes involving the nuclear envelope during cell division are similar between plants and animals, remarkable differences exist in the proteins involved. Recently, significant progress has been made to elucidate the protein constituents of the nuclear envelope and their roles in mitosis and meiosis are beginning to be revealed. While until recently, no candidate protein interactors with the nucleoskeleton had been described, the recently characterized plant SUN domain family members are strong candidates as part of a LINC complex to fulfil this role. Ongoing work in the authors' laboratory is aimed at describing the protein-binding partners of these proteins and to describe their location and function in cell division. The plant nucleoskeleton is also just yielding to investigation. Candidate proteins have been identified and the LINC mutants are yielding valuable insights, as is work using advanced microscopy. It is clear that the plant nucleoskeleton breaks down in cell division and that interactions between it and the nuclear envelope are severed; phosphorylation events and a role for cyclins are suggested. Plant NPCs resemble those of other kingdoms, but show limited sequence homology; they appear crucial to both NEBD and reformation. Once again, lack of probes and limited cloning of plant NPCs has to date made molecular dissection of plant NPCs impossible. Interestingly, Ran appears to play a crucial role in NEBD and reformation as in animal cells. Ran also plays a central role in establishing the location of the mitotic spindle and plane of division, remaining active at the point of the attachment of the PPB until the formation of the cell plate. The recent description of novel plant nuclear envelope intrinsic and associated proteins is opening up the plant nuclear envelope as a structure amenable to study. It is therefore to be expected that rapid advances will be made in the description of the plant nuclear envelope proteome and in mechanistic understanding for events in the cell cycle over the next few years. Previous SectionNext Section ACKNOWLEDGEMENTS This work was supported by a PhD studentship for K.G. and a Masters studentship for M.S. by Oxford Brookes University and a Leverhulme Trust grant (F/00382/H) funding K.G.'s post-doctoral research. , ? The Author 2011. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For Permissions, please email: journals.permissions@oup.com Previous Section LITERATURE CITED 1. ? 1. Anderson DJ, 2. Hetzer MW . Shaping the endoplasmic reticulum into the nuclear envelope. Journal of Cell Science 2008;121:137-142. Abstract/FREE Full Text 2. ? 1. Beaudouin J, 2. Gerlich D, 3. Daigle N, 4. Eils R, 5. Ellenberg J . Nuclear envelope breakdown proceeds by microtubule-induced tearing of the lamina. Cell 2002;108:83-96. CrossRefMedlineWeb of Science 3. ? 1. Bodoor K, 2. Shaikh S, 3. Salina D, 4. et al . Sequential recruitment of NPC proteins to the nuclear periphery at the end of mitosis. 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