Quantitative analysis of changes in spatial distribution and plus-end geometry of microtubules involved in plant-cell cytokinesis

Austin, Jotham R.; Seguí-Simarro, José M.; Staehelin, L. Andrew

doi:10.1242/jcs.02512

Cited by 82 publications

(84 citation statements)

References 40 publications

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“…Such a MT interdigitation phenomenon also has been shown in the moss Physcomitrella patens [17]. Although MT interdigitation was readily apparent in the endosperm phragmoplast of A. thaliana [18], the phenomenon was not obvious in its somatic cells undergoing cytokinesis [19]. Consistent with this, a dark midzone also can be seen in phragmoplast images of both anti-tubulin immunofluorescence in fixed cells and green fluorescent protein (GFP)-tubulin in live cells.…”

Section: Anti-parallel Mts In the Phragmoplastsupporting

confidence: 67%

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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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Section: Anti-parallel Mts In the Phragmoplastsupporting

confidence: 67%

“…[18], the phenomenon was not obvious in its somatic cells undergoing cytokinesis [19]. Consistent with this, a dark midzone also can be seen in phragmoplast images of both anti-tubulin immunofluorescence in fixed cells and green fluorescent protein (GFP)-tubulin in live cells.…”

Section: Anti-parallel Mts In the Phragmoplastmentioning

confidence: 56%

The rise and fall of the phragmoplast microtubule array

Lee

Liu

2013

Current Opinion in Plant Biology

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“…For example, the plus ends of most somatic phragmoplast MTs are stabilized by association with the cortex (Austin et al, 2005). EB1 and other +TIPs may regulate the association of plus ends with cortical sites in plants as in yeast and animal cells.…”

Section: Assembly Of Noncentrosomal Mt Arraysmentioning

confidence: 99%

Generation of noncentrosomal microtubule arrays

Bartolini

Gundersen

2006

Journal of Cell Science

228

219

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In most proliferating and migrating animal cells, the centrosome is the main site for microtubule (MT) nucleation and anchoring, leading to the formation of radial MT arrays in which MT minus ends are anchored at the centrosomes and plus ends extend to the cell periphery. By contrast, in most differentiated animal cell types, including muscle, epithelial and neuronal cells, as well as most fungi and vascular plant cells, MTs are arranged in noncentrosomal arrays that are non-radial. Recent studies suggest that these noncentrosomal MT arrays are generated by a three step process. The initial step involves formation of noncentrosomal MTs by distinct mechanisms depending on cell type: release from the centrosome, catalyzed nucleation at noncentrosomal sites or breakage of pre-existing MTs. The second step involves transport by MT motor proteins or treadmilling to sites of assembly. In the final step, the noncentrosomal MTs are rearranged into cell-type-specific arrays by bundling and/or capture at cortical sites, during which MTs acquire stability. Despite their relative stability, the final noncentrosomal MT arrays may still exhibit dynamic properties and in many cases can be remodeled.

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“…Our CLSM data were consistent with the idea that the chondriome of SAM and LP meristematic cells was composed of two types of mitochondria: small, discrete mitochondria in the cell periphery and a larger mitochondrial mass in the cell center whose size increased during mitosis and cytokinesis. To determine whether the mitochondrial architecture described above for SAM and LP meristematic cells is typical of all Arabidopsis cell types, we reexamined our extensive collection of EM images from different Arabidopsis cell types, including root tip, stem, mature leaf, meiocyte, microspore, pollen, endosperm, endothelial, and embryo cells Staehelin et al, 1990;Staehelin, 2000, 2004;Otegui et al, 2002Otegui et al, , 2005Otegui et al, , 2006Seguí-Simarro et al, 2004Austin et al, 2005Austin et al, , 2006Seguí-Simarro and Staehelin, 2006a;Borsics et al, 2007;Christopher et al, 2007;J.M. Seguí-Simarro and L.A. Staehelin, unpublished data).…”

Section: Mitochondria Of Living Sam and Lp Meristematic Cells Displaymentioning

confidence: 99%

The Mitochondrial Cycle of Arabidopsis Shoot Apical Meristem and Leaf Primordium Meristematic Cells Is Defined by a Perinuclear Tentaculate/Cage-Like Mitochondrion

2008

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Plant cells exhibit a high rate of mitochondrial DNA (mtDNA) recombination. This implies that before cytokinesis, the different mitochondrial compartments must fuse to allow for mtDNA intermixing. When and how the conditions for mtDNA intermixing are established are largely unknown. We have investigated the cell cycle-dependent changes in mitochondrial architecture in different Arabidopsis (Arabidopsis thaliana) cell types using confocal microscopy, conventional, and threedimensional electron microscopy techniques. Whereas mitochondria of cells from most plant organs are always small and dispersed, shoot apical and leaf primordial meristematic cells contain small, discrete mitochondria in the cell periphery and one large, mitochondrial mass in the perinuclear region. Serial thin-section reconstructions of high-pressure-frozen shoot apical meristem cells demonstrate that during G1 through S phase, the large, central mitochondrion has a tentaculate morphology and wraps around one nuclear pole. In G2, both types of mitochondria double their volume, and the large mitochondrion extends around the nucleus to establish a second sheet-like domain at the opposite nuclear pole. During mitosis, approximately 60% of the smaller mitochondria fuse with the large mitochondrion, whose volume increases to 80% of the total mitochondrial volume, and reorganizes into a cage-like structure encompassing first the mitotic spindle and then the entire cytokinetic apparatus. During cytokinesis, the cage-like mitochondrion divides into two independent tentacular mitochondria from which new, small mitochondria arise by fission. These cell cycle-dependent changes in mitochondrial architecture explain how these meristematic cells can achieve a high rate of mtDNA recombination and ensure the even partitioning of mitochondria between daughter cells.Mitochondria are the principal source of ATP energy in eukaryotic cells. Although they are often portrayed as static, oval or rod-shaped organelles that sometimes exhibit a branched configuration, studies of living cells carried out over the past 30 years have demonstrated that they are among the most plastic organelles of cells in terms of form and distribution (Calvayrac et al

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Quantitative analysis of changes in spatial distribution and plus-end geometry of microtubules involved in plant-cell cytokinesis

Cited by 82 publications

References 40 publications

The rise and fall of the phragmoplast microtubule array

The rise and fall of the phragmoplast microtubule array

Generation of noncentrosomal microtubule arrays

The Mitochondrial Cycle of Arabidopsis Shoot Apical Meristem and Leaf Primordium Meristematic Cells Is Defined by a Perinuclear Tentaculate/Cage-Like Mitochondrion

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