Functional diversification of the kinesin‐14 family in land plants

Gicking, Allison M.; Swentowsky, Kyle W.; Dawe, R. Kelly; W, Qiu

doi:10.1002/1873-3468.13094

Cited by 23 publications

(20 citation statements)

References 116 publications

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“…However, in vks1, cells at different phases of division were easily observed (Supplemental Figure 9), suggesting that mitosis in vks1 slowed down, which in turn reduced early endosperm cell proliferation (Figure 8). In addition, our data also suggested that VKS1 plays a crucial role in spindle formation and chromosome separation in plants (Figure 6), which is consistent with prior studies on plant kinesin-14s (Chen et al, 2002;Ambrose and Cyr, 2007;Higgins et al, 2016;Dawe et al, 2018;Gicking et al, 2018). The CC domain in the VKS1 N terminus is responsible for localization to MTs (Figure 3H), and the motor in the C terminus generates opposing forces on the spindle MTs, thereby pulling the daughter chromosomes equally to opposite poles of the cell.…”

Section: Vks1 Is Essential For Mt Organization In Mitosis and Cytokinsupporting

confidence: 92%

“…The kinesin-14 subfamily is greatly expanded in plants, with 20 members in Arabidopsis (Arabidopsis thaliana), 16 in rice (Oryza sativa), and 21 in maize (Supplemental Figure 1; Supplemental File), whereas only four are found in the human genome (Richardson et al, 2006). Plant kinesin-14 motors are involved in spindle morphogenesis, MT-based trafficking, chromosome segregation, chloroplast distribution, and plant-specific phragmoplast formation (Lee et al, 2015;She and Yang, 2017;Gicking et al, 2018). Arabidopsis ATK1, the first kinesin-14 protein discovered in plants, primarily functions in spindle morphogenesis and chromosome segregation during meiosis (Chen et al, 2002;Marcus et al, 2002), whereas Arabidopsis ATK5 is required for mitotic spindle pole formation (Ambrose and Cyr, 2007).…”

Section: Introductionmentioning

confidence: 99%

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Maize VKS1 Regulates Mitosis and Cytokinesis During Early Endosperm Development

et al. 2019

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Cell number is a critical factor that determines kernel size in maize (Zea mays). Rapid mitotic divisions in early endosperm development produce most of the cells that make up the starchy endosperm; however, the mechanisms underlying early endosperm development remain largely unknown. We isolated a maize mutant that shows a varied-kernel-size phenotype (vks1). Vks1 encodes ZmKIN11, which belongs to the kinesin-14 subfamily and is predominantly expressed in early endosperm development. VKS1 dynamically localizes to the nucleus and microtubules and plays key roles in the migration of free nuclei in the coenocyte as well as in mitosis and cytokinesis in early mitotic divisions. Absence of VKS1 has relatively minor effects on plants but causes deformities in spindle assembly, sister chromatid separation, and phragmoplast formation in early endosperm development, thereby resulting in reduced cell proliferation. Severities of aberrant mitosis and cytokinesis within individual vks1 endosperms differ, thereby resulting in varied kernel sizes. Our discovery highlights VKS1 as a central regulator of mitosis in early maize endosperm development and provides a potential approach for future yield improvement.

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Section: Vks1 Is Essential For Mt Organization In Mitosis and Cytokinsupporting

confidence: 92%

Section: Introductionmentioning

confidence: 99%

Maize VKS1 Regulates Mitosis and Cytokinesis During Early Endosperm Development

et al. 2019

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“…Overall, this study provides a comprehensive view on the roles of Kinesin-13 and -8 in a single plant species. Furthermore, our results reinforce the emerging view that the kinesin superfamily is well conserved in plants but have diverged in their function (Gicking et al, 2018; Nebenfuhr and Dixit, 2018).…”

Section: Discussionsupporting

confidence: 87%

Novel roles of Kinesin-13 and Kinesin-8 during cell growth and division in the mossPhyscomitrella patens

Edzuka

Goshima

et al. 2019

Preprint

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Kinesin-13 and -8 are well-known microtubule (MT) depolymerases that regulate MT length and chromosome movement in animal mitosis. While much is unknown about plant Kinesin-8, Arabidopsis and rice Kinesin-13 have been shown to depolymerise MTs in vitro. However, mitotic function of both kinesins has yet to be understood in plants. Here, we generated the complete null mutants in plants of Kinesin-13 and -8 in the moss Physcomitrella patens. Both kinesins were found to be non-essential for viability, but the Kinesin-13 knockout (KO) line had increased mitotic duration and reduced spindle length, whereas the Kinesin-8 KO line did not display obvious mitotic defects. Surprisingly, spindle MT poleward flux, for which Kinesin-13 is responsible for in animals, was retained in the absence of Kinesin-13. Concurrently, MT depolymerase activity of either moss kinesins could not be observed, with MT catastrophe inducing (Kinesin-13) or MT gliding (Kinesin-8) activity observed in vitro. Interestingly, both KO lines showed waviness in their protonema filaments, which correlated with positional instability of the MT foci in their tip cells. Taken together, the results suggest that plant Kinesin-13 and -8 have diverged in both mitotic function and molecular activity, acquiring new roles in regulating MT foci positioning for directed tip-growth.One sentence summaryThis study uncovered the roles of Kinesin-13 and Kinesin-8 in regulating microtubule dynamics for mitotic spindle formation and straight tip cell growth in the moss Physcomitrella patens

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“…This raises an additional level of regulation of α-Aurora kinases. The presence of a larger number of kinesin genes in plant genomes, in comparison to animals or humans [31,32] can explain the diversity of TPXL isoforms in the B group. At the same time, the reason for such evolutionary separation of the TPXL family based on functionality remains unclear.…”

Section: Diversity Of Tpx In Plantsmentioning

confidence: 99%

Functional Divergence of Microtubule-Associated TPX2 Family Members in Arabidopsis thaliana

Tomaštíková

Rutten

Dvořák

et al. 2020

IJMS

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TPX2 (Targeting Protein for Xklp2) is an evolutionary conserved microtubule-associated protein important for microtubule nucleation and mitotic spindle assembly. The protein was described as an activator of the mitotic kinase Aurora A in humans and the Arabidopsis AURORA1 (AUR1) kinase. In contrast to animal genomes that encode only one TPX2 gene, higher plant genomes encode a family with several TPX2-LIKE gene members (TPXL). TPXL genes of Arabidopsis can be divided into two groups. Group A proteins (TPXL2, 3, 4, and 8) contain Aurora binding and TPX2_importin domains, while group B proteins (TPXL1, 5, 6, and 7) harbor an Xklp2 domain. Canonical TPX2 contains all the above-mentioned domains. We confirmed using in vitro kinase assays that the group A proteins contain a functional Aurora kinase binding domain. Transient expression of Arabidopsis TPX2-like proteins in Nicotiana benthamiana revealed preferential localization to microtubules and nuclei. Co-expression of AUR1 together with TPX2-like proteins changed the localization of AUR1, indicating that these proteins serve as targeting factors for Aurora kinases. Taken together, we visualize the various localizations of the TPX2-LIKE family in Arabidopsis as a proxy to their functional divergence and provide evidence of their role in the targeted regulation of AUR1 kinase activity.

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Functional diversification of the kinesin‐14 family in land plants

Cited by 23 publications

References 116 publications

Maize VKS1 Regulates Mitosis and Cytokinesis During Early Endosperm Development

Maize VKS1 Regulates Mitosis and Cytokinesis During Early Endosperm Development

Novel roles of Kinesin-13 and Kinesin-8 during cell growth and division in the mossPhyscomitrella patens

Functional Divergence of Microtubule-Associated TPX2 Family Members in Arabidopsis thaliana

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