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In BriefIN BRIEF
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POK Marks the Spot: Kinesin-12 Proteins Are Spatial Markers of the Site Transiently Occupied by the Preprophase Band

Kathleen L. Farquharson
Kathleen L. Farquharson
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Published June 2014. DOI: https://doi.org/10.1105/tpc.114.128850

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  • © 2014 American Society of Plant Biologists. All rights reserved.

In 1966, Pickett-Heaps and Northcote reported that a band of microtubules encircled the nuclei of mitotic wheat cells before prophase (Pickett-Heaps and Northcote, 1966). Although this so-called preprophase band (PPB) disappeared by metaphase, it faithfully anticipated the site of the future cell plate. This finding gave rise to the hypothesis that the PPB determines the plane of cell division by recruiting molecules to the cortical division site and that these molecules guide the phragmoplast to the correct cortical sites during cytokinesis (reviewed in Rasmussen et al., 2013). Much research has focused on deciphering the mechanism by which cells keep track of the positional information of the PPB and use it to guide cell plate growth. Mutants lacking components of the guidance mechanism exhibit irregular cell shapes and organ stunting, emphasizing the importance of division plane control for plant morphology. TANGLED (TAN; a microtubule binding protein) and two kinesin-12 proteins, PHRAGMOPLAST ORIENTING KINESIN1 (POK1) and POK2, have been shown to maintain the spatial memory of the PPB and to control cell wall positioning during cytokinesis (Smith et al., 1996; Müller et al., 2006; Walker et al., 2007). TAN was shown to bind to the C terminus of POK1 in yeast two-hybrid experiments (Müller et al., 2006), and TAN localization at the cortical division zone was found to rely on POK function (Walker et al., 2007).

By combining genetic analysis and live-cell imaging, Lipka et al. (pages 2617–2632) further evaluated the role of POK1 and POK2 in mitosis. They examined a novel Arabidopsis pok2 allele (pok2-3), isolated in a screen for pok1 enhancers. Root meristem cells were haphazardly arranged in dramatically dwarfed pok1-1 pok2-3 seedlings and displayed tilting phragmoplasts that deviated from the PPB position, confirming that POK1 and POK2 are involved in the spatial control of cytokinesis. Next, the authors determined that TAN-YFP localized to the PPB in the root meristem of both wild-type and pok1-1 pok2-3 plants transgenically expressing TAN-YFP, indicating that POK function is not required for the initial localization of TAN to the PPB. However, TAN-YFP was delocalized from the PPB during metaphase in pok1-1 pok2-3 plants, but not in the wild type. Thus, POK proteins are required for TAN maintenance at the cortical division zone after PPB disintegration and are integral to the cortical division zone. Bimolecular fluorescence complementation analysis showed that TAN interacts with the C terminus of POK1 in planta, suggesting that POK1 physically anchors TAN to the cortical division zone.

Furthermore, a functional YFP fusion of POK1 localized to the cortical division zone of wild-type root meristem cells expressing YFP-POK1 throughout mitosis (see figure), suggesting that POK1 is a continuous spatial marker for the site initially occupied by the PPB. Fluorescence recovery after photobleaching analysis coupled with oryzalin-mediated microtubule destabilization demonstrated that POK1 is dynamically recruited to the PPB during prophase in a microtubule-dependent manner but that POK1 is subsequently maintained at the cortical division zone even in the absence of cortical microtubules.

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Throughout mitosis, YFP-POK1 is localized to the region initially occupied by the PPB. Arabidopsis root meristem cells coexpressing the tubulin marker RFP-MBD (magenta in the merge column) and YFP-POK1 (green in the merge column). Yellow arrows indicate the long axis of the root and white arrows show YFP-POK1 localization at the cortical division zone. Bar = 10 μm. (Adapted from Lipka et al. [2014], Figure 4B.)

The authors propose that POK proteins act as a scaffold that anchors cortical division site identity proteins, such as TAN, at the cortical division zone throughout mitosis. Future work will evaluate whether POK proteins actively guide phragmoplast formation during cytokinesis.

Footnotes

  • www.plantcell.org/cgi/doi/10.1105/tpc.114.128850

References

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    1. Lipka E.,
    2. Gadeyne A.,
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    6. Ehrhardt D.W.,
    7. Kirik V.,
    8. Van Damme D.,
    9. Müller S.
    (2014). The phragmoplast-orienting kinesin-12 class proteins translate the positional information of the preprophase band to establish the cortical division zone in Arabidopsis. Plant Cell 26: 2617–2632.
    OpenUrlAbstract/FREE Full Text
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    1. Müller S.,
    2. Han S.,
    3. Smith L.G.
    (2006). Two kinesins are involved in the spatial control of cytokinesis in Arabidopsis thaliana. Curr. Biol. 16: 888–894.
    OpenUrlCrossRefPubMed
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    1. Pickett-Heaps J.D.,
    2. Northcote D.H.
    (1966). Organization of microtubules and endoplasmic reticulum during mitosis and cytokinesis in wheat meristems. J. Cell Sci. 1: 109–120.
    OpenUrlAbstract/FREE Full Text
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    1. Rasmussen C.G.,
    2. Wright A.J.,
    3. Müller S.
    (2013). The role of the cytoskeleton and associated proteins in determination of the plant cell division plane. Plant J. 75: 258–269.
    OpenUrlCrossRefPubMed
  5. ↵
    1. Smith L.G.,
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    3. Sylvester A.W.
    (1996). The tangled-1 mutation alters cell division orientations throughout maize leaf development without altering leaf shape. Development 122: 481–489.
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  6. ↵
    1. Walker K.L.,
    2. Müller S.,
    3. Moss D.,
    4. Ehrhardt D.W.,
    5. Smith L.G.
    (2007). Arabidopsis TANGLED identifies the division plane throughout mitosis and cytokinesis. Curr. Biol. 17: 1827–1836.
    OpenUrlCrossRefPubMed
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POK Marks the Spot: Kinesin-12 Proteins Are Spatial Markers of the Site Transiently Occupied by the Preprophase Band
Kathleen L. Farquharson
The Plant Cell Jun 2014, 26 (6) 2284; DOI: 10.1105/tpc.114.128850

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POK Marks the Spot: Kinesin-12 Proteins Are Spatial Markers of the Site Transiently Occupied by the Preprophase Band
Kathleen L. Farquharson
The Plant Cell Jun 2014, 26 (6) 2284; DOI: 10.1105/tpc.114.128850
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The Plant Cell Online: 26 (6)
The Plant Cell
Vol. 26, Issue 6
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