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Preprophase-band positioning in isolated tobacco BY-2 cells: evidence for a principal role of nucleus-cell cortex interaction in default division-plane selection

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A Correction to this article was published on 10 January 2019

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Abstract

In some plant tissue types, new cross-walls tend to divide parental cells equally and to meet parental walls at right angles while tending to have minimal surface area. A previously proposed model that I call the reach model suggests that this feature originates from the tendency of premitotic division-plane selection or of the positioning of microtubule preprophase bands (PPBs) which predict the cortical division site, and that default division-plane selection involves nuclear centering and subsequent PPB microtubule assembly on the cell wall parts closest to the nucleus. In an initial effort to characterize truly default division-plane selection, the present study quantified division orientation and PPB positioning in protoplast-derived isolated elongate tobacco BY-2 cells. In this system, PPB-predicted and actual division planes were mostly oriented transversely, as predicted based on the reach model. Some sample elongate cells had asymmetric shapes that came from clear terminal-size differences and, in those cells, PPB-marked planes tended to be displaced from the centers of centrally located nuclei toward the narrower cell end, again as predicted based on the reach model. Such PPB positioning typically forecasted volumetrically asymmetric transverse division that would produce a smaller daughter cell from a parental cell part including the narrower cell end. These results provide experimental evidence that default division-plane selection tends to be close to or the same as the selection using the reach model’s criterion, and that it does not use any criterion that specifically prioritizes the equality or verticality of division.

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Change history

  • 10 January 2019

    The original version of this article unfortunately contains a mistake.

Abbreviations

mLS:

Modified Linsmaier and Skoog’s medium

PPB:

Preprophase band

S :

Cell slenderness ratio

SAI :

Shape asymmetry index

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Acknowledgements

I thank Dr. Hiroki Yasuhara for providing tobacco BY-2 cells stably expressing YFP-tubulin, and Dr. Tomohiro Akashi and Dr. Junko Katsuta-Akashi for their helpful comments on earlier versions of this manuscript.

Funding

Osaka University faculty members provided the financial and practical support.

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Authors and Affiliations

  1. Department of Biological Science, Graduate School of Science, Osaka University, Machikaneyama 1-1, Toyonaka, Osaka, 560-0043, Japan

    Tetsuhiro Asada

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  1. Tetsuhiro Asada
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Correspondence to Tetsuhiro Asada.

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Handling Editor: Anne-Catherine Schmit

Electronic supplementary material

Online Resource 1

Flowchart of image analysis procedure. Fig. 1b was prepared with shapes corresponding to g2 and g3, and Fig. 1c was prepared with shapes corresponding to g7. (DOCX 9.50 MB)

Online Resource 2

Shape-ordering with differently defined SAIs. The three example shapes are line-symmetrical trapezoids with terminally located parallel sides. Because of the simplicity of the shapes, asymmetry levels can be compared using length-measurement-based SAIs, such as the terminal-size ratio and the ratio of the difference in terminal size to the major-axis length, referred to as the narrowing rate. As shown in this figure, shape ordering by the terminal-size ratio and narrowing rate can provide different results, and the definition used in the present study, SAI = 100 × (A′ − A)/(A × S), leads to an ordering similar to one by the narrowing rate. SAI can also be defined as being proportional only to (A′ − A)/A. Shape-ordering with this alternative definition tends to suggest markedly higher asymmetry levels for elongated cells and, in this respect, it is similar to that based on the terminal-size ratio, as explained in this Fig. A cell sample’s silhouette area; A’ area of the union of the cell sample’s silhouette and its 180-degree rotation around the centroid; S cell slenderness ratio. Each M indicates the highest value, and brackets connect the same or closest values. (DOCX 1.62 MB)

Online Resource 3

Frequency distributions of the division-line angle obtained for four groups of collected cell samples with PPBs that differed in the level of SAI (a) or cell area size (b). Each angle was measured in respect to the parental cell silhouette’s approximate ellipse’s major axis. S cell slenderness ratio (see Fig. 1b). (DOCX 8.47 MB)

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Asada, T. Preprophase-band positioning in isolated tobacco BY-2 cells: evidence for a principal role of nucleus-cell cortex interaction in default division-plane selection. Protoplasma 256, 721–729 (2019). https://doi.org/10.1007/s00709-018-01331-5

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