Mitosis-specific kinesins in Arabidopsis

Vanstraelen, Marleen; Inzé, Dirk; Geelen, Danny

doi:10.1016/j.tplants.2006.02.004

Cited by 70 publications

(74 citation statements)

References 88 publications

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“…Given these four kinesin-5 genes, it is reasonable to predict some functional redundancy, especially since AtKRP125a, b and c are all upregulated during mitosis (Vanstraelen et al, 2006). The persistence of some normal spindles in rsw7 at the restrictive temperature might indicate partial redundancy between AtKRP125c and another kinesin-5 motor, or with structural spindle proteins, such as AtMAP65, which localizes to the spindle midline at anaphase (Mao et al, 2005).…”

Section: Discussionmentioning

confidence: 99%

A conserved role for kinesin-5 in plant mitosis

Bannigan

Scheible

Lukowitz

et al. 2007

Journal of Cell Science

108

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The mitotic spindle of vascular plants is assembled and maintained by processes that remain poorly explored at a molecular level. Here, we report that AtKRP125c, one of four kinesin-5 motor proteins in arabidopsis, decorates microtubules throughout the cell cycle and appears to function in both interphase and mitosis. In a temperature-sensitive mutant, interphase cortical microtubules are disorganized at the restrictive temperature and mitotic spindles are massively disrupted, consistent with a defect in the stabilization of anti-parallel microtubules in the spindle midzone, as previously described in kinesin-5 mutants from animals and yeast. AtKRP125c introduced into mammalian epithelial cells by transfection decorates microtubules throughout the cell cycle but is unable to complement the loss of the endogenous kinesin-5 motor (Eg5). These results are among the first reports of any motor with a major role in anastral spindle structure in plants and demonstrate that the conservation of kinesin-5 motor function throughout eukaryotes extends to vascular plants.

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Section: Discussionmentioning

confidence: 99%

A conserved role for kinesin-5 in plant mitosis

Bannigan

Scheible

Lukowitz

et al. 2007

Journal of Cell Science

108

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“…The best studied kinesin-14 members are Drosophila Ncd (Komma et al, 1991;Matthies et al, 1996) and Saccharomyces cerevisiae Kar3 (Meluh and Rose, 1990). These MT motors, and their mammalian (Matuliene et al, 1999;Mountain et al, 1999;Zhu et al, 2005) and plant (Vanstraelen et al, 2006) homologues, play essential roles in mitosis and meiosis. Their activities are important for the formation of the mitotic spindle poles (Goshima and Vale, 2003; MoralesMulia and Scholey, 2005;Zhu et al, 2005) and for regulation of the distance between the poles in the mitotic spindle (Saunders and Hoyt, 1992;Saunders et al, 1997;Sharp et al, 1999Sharp et al, , 2000aTroxell et al, 2001).…”

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confidence: 99%

Microtubule Motor Ncd Induces Sliding of Microtubules In Vivo

Oladipo

Cowan

Rodionov

2007

MBoC

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The mitotic spindle is a microtubule (MT)-based molecular machine that serves for equal segregation of chromosomes during cell division. The formation of the mitotic spindle requires the activity of MT motors, including members of the kinesin-14 family. Although evidence suggests that kinesins-14 act by driving the sliding of MT bundles in different areas of the spindle, such sliding activity had never been demonstrated directly. To test the hypothesis that kinesins-14 can induce MT sliding in living cells, we developed an in vivo assay, which involves overexpression of the kinesin-14 family member Drosophila Ncd in interphase mammalian fibroblasts. We found that green fluorescent protein (GFP)-Ncd colocalized with cytoplasmic MTs, whose distribution was determined by microinjection of Cy3 tubulin into GFPtransfected cells. Ncd overexpression resulted in the formation of MT bundles that exhibited dynamic "looping" behavior never observed in control cells. Photobleaching studies and fluorescence speckle microscopy analysis demonstrated that neighboring MTs in bundles could slide against each other with velocities of 0.1 m/s, corresponding to the velocities of movement of the recombinant Ncd in in vitro motility assays. Our data, for the first time, demonstrate generation of sliding forces between adjacent MTs by Ncd, and they confirm the proposed roles of kinesins-14 in the mitotic spindle morphogenesis. INTRODUCTIONThe mitotic spindle is a molecular machine that serves for equal segregation of chromosomes during mitosis. The principal structural components of the mitotic spindle are cytoplasmic microtubules (MTs) organized into two polarized (minus ends at the center) radial arrays, located at a distance from each other. MT organization in the mitotic spindle is achieved by MT motors, kinesins and dyneins, which generate force for movement toward the plus or minus ends of MTs and that participate in the transport of chromosomes to the spindle poles, spindle elongation during anaphase, regulation of the MT turnover rates, and spindle morphogenesis (for review, see Sharp et al., 2000b;Karsenti and Vernos, 2001;McIntosh et al., 2002;Scholey et al., 2003;Gadde and Heald, 2004;Wadsworth and Khodjakov, 2004).A special role in the formation and maintenance of the mitotic spindle belongs to the minus-end-directed members of the kinesin-14 subfamily. Unlike conventional kinesin, kinesin-14 family members have motor domains at the carboxy terminus (for review, see Ovechkina and Wordeman, 2003). The best studied kinesin-14 members are Drosophila Ncd (Komma et al., 1991;Matthies et al., 1996) and Saccharomyces cerevisiae Kar3 (Meluh and Rose, 1990). These MT motors, and their mammalian (Matuliene et al., 1999;Mountain et al., 1999;Zhu et al., 2005) and plant (Vanstraelen et al., 2006) homologues, play essential roles in mitosis and meiosis. Their activities are important for the formation of the mitotic spindle poles (Goshima and Vale, 2003; MoralesMulia and Scholey, 2005;Zhu et al., 2005) and for regulation of the distance...

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“…The kinesin coded for by At1g55550 clusters with kinesin-4s, which are involved in chromosome segregation and At1g55550 has not been listed among the mitotic kinesins. 23 Whether this observation reflects a more specific role for At1g55550 in competing with and thereby blocking the action of kinesins involved in conventional spindle assembly and/or phragmoplast formation needs to be elucidated in a comprehensive study. The kinesin ATK4 (At5g27000) is reported to be expressed during the mitotic phase in synchronized Arabidopsis cell culture.…”

Section: Uncharacterized Genes With Strong Endosperm Expressionmentioning

confidence: 99%

“…The kinesin ATK4 (At5g27000) is reported to be expressed during the mitotic phase in synchronized Arabidopsis cell culture. [23][24][25] Like ATK1, ATK4-like and ATK5, ATK4 clusters with the kinesin-14s, characterized by their C-terminal the specialized radial microtubule systems and cytokinetic phragmoplasts are absent. 15 This study also indicates that the MAPS, MAP65-1 and AtEB1c, may also play important roles that are specific to early endosperm development.…”

Section: Uncharacterized Genes With Strong Endosperm Expressionmentioning

confidence: 99%

Identification of cytoskeleton-associated genes expressed during Arabidopsis syncytial endosperm development

Day

Müller

Macknight

2009

Plant Signaling & Behavior

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During the early stages of Arabidopsis seed development, the endosperm is syncytial and proliferates rapidly through multiple rounds of mitosis in the absence of cytokinesis and cell wall formation. This stage of endosperm development is important in determining seed viability and size. To identify genes involved in syncytial endosperm development, we analyzed the endosperm transcriptome, obtained using laser capture microdissection of developing seeds at four days after pollination. Our results support the idea that similar sets of genes are required for conventional somatic mitosis with cytokinesis and syncytial proliferation. Furthermore, we identify cytoskeleton associated genes that may act to facilitate syncytial development thereby providing an important resource for further characterization of the processes involved in syncytial endosperm development.Seed development begins with double fertilization where the haploid egg cell and the double haploid central cell are both fertilized by haploid sperm cells contributed from a single pollen grain. This generates the diploid embryo and the triploid endosperm, respectively. The embryo and the endosperm grow rapidly in a coordinated manner that is influenced by the surrounding maternal integument tissues that later form the seed coat. During these early stages, maternal resources are used for the rapid cell division and growth that occurs as seed tissues form and develop. In many plant species, including Arabidopsis, the triploid primary endosperm nucleus undergoes several rounds of free-nuclear division, growing rapidly as a syncytium. The organization of microtubule arrays during this early stage of endosperm development is markedly different from those found in vegetative tissues.1 During the syncytial phase, interphase microtubules emanate from the nucleus into the cytoplasm and this nucleus-based radial microtubule system aids in positioning of nuclei and the designation of cytoplasm into nucleo-cytoplasmic domains. At about six days after pollination, cell wall deposition is initiated by the formation of phragmoplasts at the margins of nucleocytoplasmic domains. Interestingly, interzonal arrays which resemble phragmoplasts form between nuclei after karyokinesis, but they never participate in cell plate formation.2 This unusual form of cellular development is conducive to a rapid cellular proliferation; however, the molecular mechanisms that underlie the uncoupling of cell wall formation from mitosis remain elusive.To gain further insights into the early stages of endosperm biology, we have used laser capture microdissection to obtain RNA from syncytial stage endosperm at four days after pollination. At this stage of development, the endosperm has undergone six to seven rounds of nuclear division (~200 nucleocytoplasmic domains) but has not cellularized and the embryo is at the globular phase. Endosperm RNA was amplified using two-round in vitro transcription, then labeled and used, along with similarly treated silique amplified RNA, to probe long oligonucl...

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Mitosis-specific kinesins in Arabidopsis

Cited by 70 publications

References 88 publications

A conserved role for kinesin-5 in plant mitosis

A conserved role for kinesin-5 in plant mitosis

Microtubule Motor Ncd Induces Sliding of Microtubules In Vivo

Identification of cytoskeleton-associated genes expressed during Arabidopsis syncytial endosperm development

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