Two Kinesins Are Involved in the Spatial Control of Cytokinesis in Arabidopsis thaliana

Kinesins are microtubule (MT)-based motor proteins that have been identified in every eukaryotic species. Intriguingly, land plants have more than 60 kinesins in their genomes, many more than that in yeasts or animals. However, many of these have not yet been characterized, and their cellular functions are unknown. Here, by using endogenous tagging, we comprehensively determined the localization of 72 kinesins during mitosis in the moss Physcomitrella patens. We found that 43 kinesins are localized to mitotic structures such as kinetochores, spindle MTs, or phragmoplasts, which are MT-based structures formed during cytokinesis. Surprisingly, only one of them showed an identical localization pattern to the animal homolog, and many were enriched at unexpected sites. RNA interference and live-cell microscopy revealed postanaphase roles for kinesin-5 in spindle/phragmoplast organization, chromosome segregation, and cytokinesis, which have not been observed in animals. Our study thus provides a list of MTbased motor proteins associated with the cell division machinery in plants. Furthermore, our data challenge the current generalization of determining mitotic kinesin function based solely on studies using yeast and animal cells.

Section: Discussionmentioning

confidence: 94%

Endogenous localizome identifies 43 mitotic kinesins in a plant cell

Miki

Naito

Nishina

et al. 2014

“…Moreover, the capacity of hKif15 to drive formation of parallel bundles could explain the reported role for Caenorhabditis elegans Kinesin-12 (KLP-18) in converting disordered microtubules that are present around meiotic chromosomes into an ordered parallel array (29,30). Intriguingly, Kinesin-12s may have more diverse roles with emerging evidence suggesting that these motors are important for shaping parallel microtubule arrays within developing neuronal axons (31) and execution of cytokinesis in angiosperms (32)(33)(34). Thus, the capacity for Kinesin-12 family members to remodel dynamic microtubule networks is likely to be crucial in multiple biological systems, and it will be interesting to investigate whether they use the same mechanism.…”

Section: Discussionmentioning

confidence: 99%

Kinesin-12 motors cooperate to suppress microtubule catastrophes and drive the formation of parallel microtubule bundles

Drechsler

McAinsh

2016

Human Kinesin-12 (hKif15) plays a crucial role in assembly and maintenance of the mitotic spindle. These functions of hKif15 are partially redundant with Kinesin-5 (Eg5), which can cross-link and drive the extensile sliding of antiparallel microtubules. Although both motors are known to be tetramers, the functional properties of hKif15 are less well understood. Here we reveal how single or multiple Kif15 motors can cross-link, transport, and focus the plusends of intersecting microtubules. During transport, Kif15 motors step simultaneously along both microtubules with relative microtubule transport driven by a velocity differential between motor domain pairs. Remarkably, this differential is affected by the underlying intersection geometry: the differential is low on parallel and extreme on antiparallel microtubules where one motor domain pair becomes immobile. As a result, when intersecting microtubules are antiparallel, canonical transport of one microtubule along the other is allowed because one motor is firmly attached to one microtubule while it is stepping on the other. When intersecting microtubules are parallel, however, Kif15 motors can drive (biased) parallel sliding because the motor simultaneously steps on both microtubules that it cross-links. These microtubule rearrangements will focus microtubule plus-ends and finally lead to the formation of parallel bundles. At the same time, Kif15 motors cooperate to suppress catastrophe events at polymerizing microtubule plus-ends, raising the possibility that Kif15 motors may synchronize the dynamics of bundles that they have assembled. Thus, Kif15 is adapted to operate on parallel microtubule substrates, a property that clearly distinguishes it from the other tetrameric spindle motor, Eg5.Kinesin-12 | Kif15 | mitosis | mitotic spindle

“…Two related kinesins, PHRAGMO-PLAST-ORIENTING KINESINS 1 and 2 (POK1 and POK2) were found to interact with TANGLED and a pok1 pok2 double mutant resembles the maize tan mutant in terms of misoriented division planes (9). Although the data suggest a role for kinesins and the pioneer protein TANGLED in division-plane definition, the molecular mechanism of the process remains unknown.…”

mentioning

confidence: 97%

RanGAP1 is a continuous marker of the Arabidopsis cell division plane

Zhao

Rodrigo-Peiris

et al. 2008

Self Cite

119

166

In higher plants, the plane of cell division is faithfully predicted by the preprophase band (PPB). The PPB, a cortical ring of microtubules and F-actin, disassembles upon nuclear-envelope breakdown. During cytokinesis, the expanding cell plate fuses with the plasma membrane at the cortical division site, the site of the former PPB. The nature of the ''molecular memory'' that is left behind by the PPB and is proposed to guide the cell plate to the cortical division site is unknown. RanGAP is the GTPase activating protein of the small GTPase Ran, which provides spatial information for nucleocytoplasmic transport and various mitotic processes in animals. Here, we show that, in dividing root cells, Arabidopsis RanGAP1 concentrates at the PPB and remains associated with the cortical division site during mitosis and cytokinesis, requiring its N-terminal targeting domain. In a fass/ton2 mutant, which affects PPB formation, RanGAP1 recruitment to the PPB site is lost, while its PPB retention is microtubule-independent. RanGAP1 persistence at the cortical division site, but not its initial accumulation at the PPB requires the 2 cytokinesis-regulating kinesins POK1 and POK2. Depletion of RanGAP by inducible RNAi leads to oblique cell walls and cell-wall stubs in root cell files, consistent with cytokinesis defects. We propose that Arabidopsis RanGAP, a continuous positive protein marker of the plant division plane, has a role in spatial signaling during plant cell division.cytokinesis ͉ Ran cycle ͉ preprophase band ͉ nuclear pore