The Plant Microtubule-Associated Protein AtMAP65-3/PLE Is Essential for Cytokinetic Phragmoplast Function

Müller, Sabine; Smertenko, Andrei; Wagner, Vera; Heinrich, Maria; Hussey, Patrick J.; Hauser, Marie‐Theres

doi:10.1016/j.cub.2004.02.032

Cited by 179 publications

(189 citation statements)

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“…Members of the MAP65 protein family are required for cytokinesis in human, Drosophila, and Arabidopsis (Jiang et al 1998;Mollinari et al 2002;Müller et al 2004;Vernì et al 2004). Thus, our data suggest that phosphorylation of Thr-579 in NtMAP65-1 by NRK1/NTF6 MAPK is a key reaction that controls the functions of NtMAP65-1a during cytokinesis.…”

Section: Phosphorylation Of Thr-579 In Ntmap65-1a By Nrk1/ntf6 Mapk Imentioning

confidence: 99%

“…Thus, our data suggest that phosphorylation of Thr-579 in NtMAP65-1 by NRK1/NTF6 MAPK is a key reaction that controls the functions of NtMAP65-1a during cytokinesis. Various members of the MAP65 family are concentrated at the phragmoplast in a variety of plants (Smertenko et al 2000Müller et al 2004;Van Damme et al 2004a). Both AtMAP65-1 and AtMAP65-2 of Arabidopsis, which are the most strongly homologous to members of the tobacco NtMAP65-1 family among MAP65 isotypes, and AtMAP65-3 are also phosphorylated by NRK1/NTF6 (our unpublished data).…”

Section: Phosphorylation Of Thr-579 In Ntmap65-1a By Nrk1/ntf6 Mapk Imentioning

confidence: 99%

“…Our results provide some information that might help to answer this question. Members of the MAP65 family might play a role in the maintenance of the central spindle in animals (Jiang et al 1998;Mollinari et al 2002;Verbrugghe and White 2004;Vernì et al 2004) and the phragmoplast in plants during cytokinesis (Smertenko et al 2000;Müller et al 2004). Some members might also be involved in the bundling of MTs in vivo to stabilize and maintain functional central spindles or phragmoplasts (Fig.…”

Section: Mapk Might Accelerate Expansion Of the Phragmoplast Via Phosmentioning

confidence: 99%

“…Members of this family are concentrated at the midzone of the central spindle and the phragmoplast during cytokinesis, and their appropriate organization seems to be required for completion of cytokinesis (Pellman et al 1995;Juang et al 1997;Jiang et al 1998;Mollinari et al 2002;Schuyler et al 2003;Müller et al 2004;Verbrugghe and White 2004;Vernì et al 2004). PRC1 is phosphorylated by cyclin-dependent protein kinases (CDKs), and overexpression of a mutant form of PRC1 that cannot be phosphorylated by CDKs results in the bundling of the MTs of the metaphase spindle and interruption of the progression from metaphase to anaphase, suggesting that phosphorylation of PRC1 by CDKs is required for the metaphase-to-anaphase transition (Mollinari et al 2002).…”

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Phosphorylation of NtMAP65-1 by a MAP kinase down-regulates its activity of microtubule bundling and stimulates progression of cytokinesis of tobacco cells

Sasabe¹,

Soyano²,

Takahashi³

et al. 2006

Genes Dev.

170

177

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The tobacco mitogen-activated protein kinase (MAPK) cascade, which includes MAPK NRK1/NTF6, positively regulates expansion of the cytokinetic machinery known as the phragmoplast, which is followed by the synthesis of cell plates for completion of cell division. However, molecular events lying between the MAPK and phragmoplast expansion were not known. Here, we show that NRK1/NTF6 phosphorylates the threonine residue at position 579 in NtMAP65-1a, a microtubule-associated (MT-associated) protein. Levels of phosphorylated NtMAP65-1 increase during late M phase of the cell cycle, when NRK1/NTF6 is activated. Phosphorylated NtMAP65-1 is concentrated at the equator of phragmoplast, as is NRK1/NTF6. Overexpression of mutant forms of NtMAP65-1a that cannot be phosphorylated by NRK1 delays progression of the M phase and phragmoplast expansion, also rendering phragmoplast structures resistant to an MT-depolymerizing drug. Phosphorylation of NtMAP65-1 by NRK1/NTF6 down-regulates its MT-bundling activity in vitro. These results suggest that phosphorylation of NtMAP65-1 by NRK1/NTF6 also reduces its MT-bundling activity in vivo, which enhances destabilization and turnover of MTs at the phragmoplast equator, perhaps facilitating phragmoplast expansion.[Keywords: MAP65/PRC1; MAPK; cytokinesis; microtubule; microtubule-associated proteins; phragmoplast] Supplemental material is available at http://www.genesdev.org. Cell division in eukaryotes requires dynamic changes in cytoskeletal structures that consist of microtubules (MTs) and microfilaments Jürgens 2005). During cytokinesis, the final critical step in the cell division, cells form a cytokinesis-specific apparatus (known as the central spindle in animals and the phragmoplast in plants) that plays a key role in cytokinesis (Field et al. 1999;. These structures develop from late anaphase to telophase between the two daughter nuclei, and consist of two bundles of antiparallel MTs. As cytokinesis proceeds, the central spindle becomes compacted in animal cells and the phragmoplast expands centrifugally in plant cells, and new membranes and/or cell walls are generated inside or outside the midzone of the central spindle or the phragmoplast to separate the two daughter cells from each other (Otegui et al. 2005). These dynamic processes appear to be mediated by the turnover of MTs, which involves the depolymerization of MTs and the polymerization of tubulin at the plus ends (Shelden and Wadsworth 1990;Asada et al. 1991;Hush et al. 1994;Straight and Field 2000). Recently, Austin et al. (2005) have reported that somatic-type phragmoplast MTs do not interdigitate at the cell plate mid-line and that distinct MT plus-end geometries are seen during the different stages of cytokinesis.The members of the MAP65/Ase1/PRC1 family (designated the MAP65 family herein)-including plant MAP65, yeast Ase1, and human PRC1-participate in the bundling of MTs (Chang-Jie and Sonobe 1993;Chan et al. 1999;Mollinari et al. 2002;Schuyler et al. 2003;

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Section: Phosphorylation Of Thr-579 In Ntmap65-1a By Nrk1/ntf6 Mapk Imentioning

confidence: 99%

Section: Phosphorylation Of Thr-579 In Ntmap65-1a By Nrk1/ntf6 Mapk Imentioning

confidence: 99%

Section: Mapk Might Accelerate Expansion Of the Phragmoplast Via Phosmentioning

confidence: 99%

mentioning

confidence: 99%

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Phosphorylation of NtMAP65-1 by a MAP kinase down-regulates its activity of microtubule bundling and stimulates progression of cytokinesis of tobacco cells

Sasabe¹,

Soyano²,

Takahashi³

et al. 2006

Genes Dev.

170

177

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“…Interdigitation is mainly brought about by the MT cross-linker MAP65-3, a cytokinesis specific member of the evolutionarily conserved MAP65/Ase1 family including PRC1 in humans [6 ,21]. Loss of MAP65-3 causes a widened phragmoplast midzone, likely due to the disappearance of interdigitating MTs, and frequent failures in cytokinesis [22]. Currently, it is unclear how the phragmoplast MT array maintains its bipolar appearance without MAP65-3.…”

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confidence: 99%

The rise and fall of the phragmoplast microtubule array

Lee

Liu

2013

Current Opinion in Plant Biology

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The cytokinetic apparatus, the phragmoplast, contains a bipolar microtubule (MT) framework that has the MT plus ends concentrated at or near the division site. This anti-parallel MT array provides tracks for the transport of Golgi-derived vesicles toward the plus ends so that materials enclosed are subsequently deposited at the division site. Here we will discuss a proposed model of the centrifugal expansion of the phragmoplast that takes place concomitantly with the assembly of the cell plate, the ultimate product of vesicle fusion. The expansion is a result of continuous MT assembly at the phragmoplast periphery while the MTs toward the center of the phragmoplast are disassembled. These events are the result of MT-dependent MT polymerization, bundling of antiparallel MTs coming from opposite sides of the division plane that occurs selectively at the phragmoplast periphery, positioning of the plus ends of cross-linked MTs at or near the division site by establishing a minimal MT-overlapping zone, and debundling of anti-parallel MTs that is triggered by phosphorylation of MT-associated proteins. The debundled MTs are disassembled at last by factors including the MT severing enzyme katanin. IntroductionThe innovation of the phragmoplast marks a significant advancement in the evolution from green algae to land plants [1]. The phragmoplast contains a core of two mirrored sets of anti-parallel microtubules (MTs) whose plus ends are concentrated at or near the midzone of this cytokinetic apparatus (Figure 1) [2]. The ultimate mission of this bipolar MT array is to allow Golgi-derived vesicles to be transported unidirectionally toward MT plus ends so that the materials enclosed in these vesicles are deposited for the assembly of the cell plate. Phragmoplast MTs, like those MTs in spindles during mitosis, undergo continuous remodeling throughout cytokinesis [3,4]. Upon the completion of anaphase, MTs are polymerized and coalesced in the spindle midzone, and a bipolar array is established as the Kinesin-5 motor acts on anti-parallel MTs to slide them against each other ( Figure 1a) [5,6 ,7]. Concomitant with the addition of more MTs to the array, the MTs are shortened at their minus ends, which are facing the reforming daughter nuclei (Figure 1b). One of the most spectacular phenomena in cytokinesis is the centrifugal expansion of the phragmoplast MT array from the cell center to the edge. During the expansion, new MT filaments are added to the periphery of the phragmoplast while older ones in the inner part of the phragmoplast array are disassembled ( Figure 1c). This is particularly challenging because those opposing activities occur simultaneously within a few microns of each other. The assembly of new MTs uses tubulin subunits released from the depolymerization of older MTs [3].Before MT-associated proteins (MAPs) and MT-based motors were identified, microscopic observations had revealed many structural details of the phragmoplast in elegant systems like the endosperm of the African blood lily Haemanthus and tobacc...

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Plant Cell Division

Müller

2012

Encyclopedia of Life Sciences

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Cell division is characterised by the segregation of genetic material and the redistribution of cellular contents facilitated by the cytoskeleton. Plant cells derive from divisions in the meristems of developing organs. However, plant cells are enclosed in rigid cell walls, unable to migrate and change their location within tissues. Thus, positions of division planes, together with successive polarised cell expansion are the major determinants of cell shape and consequently morphology of plants. The basic building blocks of the cytoskeleton, tubulins, actins and cytoskeleton associated motor‐ and nonmotor‐proteins are conserved. Yet, plants have developed unique cytoskeletal arrays and molecular mechanism to determine the division plane very early in mitosis and to facilitate the synthesis and insertion of the partitioning cell plate at the end of cell division. Key Concepts: Plant cells utilise specialised cytoskeletal arrays to determine the division plane early in mitosis and form a cell plate to separate daughter cells late in mitosis. Cell geometry and nuclear position are informative for division plane selection. The preprophase band (PPB) predicts the future division plane and recruits proteins that identify the cortical division site (CDS) throughout mitosis. Mutants defective in PPB or CDS establishment/maintenance exhibit mispositioned cell walls and altered cell and plant morphology. Successful cell plate formation relies on cytoskeletal reorganisation and vesicle fusion.

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The Plant Microtubule-Associated Protein AtMAP65-3/PLE Is Essential for Cytokinetic Phragmoplast Function

Cited by 179 publications

References 23 publications

Phosphorylation of NtMAP65-1 by a MAP kinase down-regulates its activity of microtubule bundling and stimulates progression of cytokinesis of tobacco cells

Phosphorylation of NtMAP65-1 by a MAP kinase down-regulates its activity of microtubule bundling and stimulates progression of cytokinesis of tobacco cells

The rise and fall of the phragmoplast microtubule array

Plant Cell Division

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