Advertisement

Protoplasma

pp 1–9 | Cite as

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

  • Tetsuhiro AsadaEmail author
Original Article
  • 127 Downloads

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.

Keywords

Cell division plane Cell wall Microtubule Preprophase band 

Abbreviations

mLS

Modified Linsmaier and Skoog’s medium

PPB

Preprophase band

S

Cell slenderness ratio

SAI

Shape asymmetry index

Notes

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 information

Osaka University faculty members provided the financial and practical support.

Compliance with ethical standards

Conflict of interest

The author declares that they have no conflict of interest.

Supplementary material

709_2018_1331_MOESM1_ESM.docx (9.5 mb)
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)
709_2018_1331_MOESM2_ESM.docx (1.6 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)
709_2018_1331_MOESM3_ESM.docx (8.5 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)

References

  1. Abe T, Hashimoto T (2005) Altered microtubule dynamics by expression of modified α-tubulin protein causes right-handed helical growth in transgenic Arabidopsis plants. Plant J 43:191–204CrossRefGoogle Scholar
  2. Abrash EB, Bergmann DC (2009) Asymmetric cell divisions: a view from plant development. Dev Cell 16:783–796CrossRefGoogle Scholar
  3. Asada T (2013) Division of shape-standardized tobacco cells reveals a limit to the occurrence of single-criterion-based selection of the plane of symmetric division. Plant Cell Physiol 54:827–837.  https://doi.org/10.1093/pcp/pct044 CrossRefGoogle Scholar
  4. Barbier de Reuille P, Routier-Kierzkowska AL, Kierzkowski D, Bassel GW, Schüpbach T, Tauriello G, Bajpai N, Strauss S, Weber A, Kiss A, Burian A, Hofhuis H, Sapala A, Lipowczan M, Heimlicher MB, Robinson S, Bayer EM, Basler K, Koumoutsakos P, Roeder AH, Aegerter-Wilmsen T, Nakayama N, Tsiantis M, Hay A, Kwiatkowska D, Xenarios I, Kuhlemeier C, Smith RS (2015) MorphoGraphX: a platform for quantifying morphogenesis in 4D. eLife 4:05864.  https://doi.org/10.7554/eLife.05864.001 CrossRefGoogle Scholar
  5. Bassel GW, Stamm P, Mosca G, Barbier de Reuille P, Gibbs DJ, Winter R, Janka A, Holdsworth MJ, Smith RS (2014) Mechanical constraints imposed by 3D cellular geometry and arrangement modulate growth patterns in the Arabidopsis embryo. Proc Natl Acad Sci U S A 111:8685–8690.  https://doi.org/10.1073/pnas.1404616111 CrossRefGoogle Scholar
  6. Besson S, Dumais J (2011) Universal rule for the symmetric division of plant cells. Proc Natl Acad Sci U S A 108:6294–6299.  https://doi.org/10.1073/pnas.1011866108 CrossRefGoogle Scholar
  7. Dupuy L, Mackenzie J, Haseloff J (2010) Coordination of plant cell division and expansion in a simple morphogenetic system. Proc Natl Acad Sci U S A 107:2711–2716CrossRefGoogle Scholar
  8. Errera L (1888) Über zellformen und seifenblasen. Bot Centralbl 34:395–398Google Scholar
  9. Flanders DJ, Rawlins DJ, Shaw PJ, Lloyd CW (1990) Nucleus-associated microtubules help determine the division plane of plant epidermal cells: avoidance of 4-way junctions and the role of cell geometry. J Cell Biol 110:1111–1122CrossRefGoogle Scholar
  10. Green P, Selker JML (1991) Mutual alignments of cell walls, cellulose, and cytoskeleton: their role in meristems. In: Lloyd CW (ed) The cytoskeletal basis of plant growth and form. Academic Press, London, pp 303–322Google Scholar
  11. Gunning BES (1982) The cytokinetic apparatus: its development and spatial regulation. In: Lloyd CW (ed) The cytoskeleton in plant growth and development. Academic Press, London, pp 229–291Google Scholar
  12. Hasezawa S, Hogetsu T, Syono K (1988) Rearrangement of cortical microtubules in elongating cells derived from tobacco protoplasts—a time-course observation by immunofluorescence microscopy. J Plant Physiol 133:46–51CrossRefGoogle Scholar
  13. Hush JM, Hawes CR, Overall RL (1990) Interphase microtubule reorientation predicts a new cell polarity in wounded pea roots. J Cell Sci 96:47–61Google Scholar
  14. Katsuta J, Hashiguchi Y, Shibaoka H (1990) The role of the cytoskeleton in positioning of the nucleus in premitotic tobacco BY-2 cells. J Cell Sci 95:413–422Google Scholar
  15. Kropf DL (1997) Induction of polarity in fucoid zygotes. Plant Cell 9:1011–1020CrossRefGoogle Scholar
  16. Lee-Stadelmann Y, Stadelmann EJ (1989) Plasmolysis and deplasmolysis. In: Fleischer B, Fleischer B (eds) Method in enzymology. Academic Press, London, pp 225–246Google Scholar
  17. Lintilhac PM (1987) Plant cytomechanics and its relationship to the development of form. In: Bereiter-Hahn J, Anderson OR, Reif WE (eds) Cytomechanics. Springer-Verlag, Berlin Heidelberg, pp 230–241CrossRefGoogle Scholar
  18. Lintilhac PM (2014) The problem of morphogenesis: unscripted biophysical control systems in plants. Protoplasma 251:25–36.  https://doi.org/10.1007/s00709-013-0522-y CrossRefGoogle Scholar
  19. Lloyd CW (1991) How does the cytoskeleton read the laws of geometry in aligning the division plane of plant-cells? Development 113(Suppl 1):55–65Google Scholar
  20. Lloyd CW, Venverloo CJ, Goodbody KC, Shaw PJ (1992) Confocal laser microscopy and 3-dimensional reconstruction of nucleus-associated microtubules in the division plane of vacuolated plant-cells. J Microsc 166:99–109CrossRefGoogle Scholar
  21. Louveaux M, Julien JD, Mirabet V, Boudaoud A, Hamant O (2016) Cell division plane orientation based on tensile stress in Arabidopsis thaliana. Proc Natl Acad Sci U S A 113:E4294–E4303.  https://doi.org/10.1073/pnas.1600677113 CrossRefGoogle Scholar
  22. Lynch TM, Lintilhac PM (1997) Mechanical signals in plant development: a new method for single cell studies. Dev Biol 181:246–256CrossRefGoogle Scholar
  23. Mineyuki Y (1999) The preprophase band of microtubules: its function as a cytokinetic apparatus in higher plants. Int Rev Cytol 187:1–49CrossRefGoogle Scholar
  24. Mineyuki Y, Mark J, Palevitz BA (1991) Relationship between the preprophase band, nucleus and spindle in dividing Allium cotyledon cells. J Plant Physiol 138:640–649CrossRefGoogle Scholar
  25. Murata T, Wada M (1991) Effects of centrifugation on preprophase-band formation in Adiantum protonemata. Planta 183:391–398CrossRefGoogle Scholar
  26. Nagata T, Takebe I (1970) Cell wall regeneration and cell division in isolated tobacco mesophyll protoplasts. Planta 92:301–308CrossRefGoogle Scholar
  27. Nagata T, Nemoto Y, Hasezawa S (1992) Tobacco BY-2 cell line as the Hela cell in the cell biology of higher-plants. Int Rev Cytol 132:1–30CrossRefGoogle Scholar
  28. Niklas KJ, Kutschera U (2012) Plant development, auxin, and the subsystem incompleteness theorem. Front Plant Sci 3:37.  https://doi.org/10.3389/fpls.2012.00037 CrossRefGoogle Scholar
  29. Petricka JJ, Van Norman JM, Benfey PN (2009) Symmetry breaking in plants: molecular mechanisms regulating asymmetric cell divisions in arabidopsis. Cold Spring Harb Perspect Biol 1:a000497CrossRefGoogle Scholar
  30. Quatrano RS (1978) Development of cell polarity. Ann Rev Plant Physiol 29:487–510CrossRefGoogle Scholar
  31. Rasmussen CG, Humphries JA, Smith LG (2011) Determination of symmetric and asymmetric division planes in plant cells. Annu Rev Plant Biol 62:387–409.  https://doi.org/10.1146/annurev-arplant-042110-103802 CrossRefGoogle Scholar
  32. Rasmussen CG, Wright AJ, Müller S (2013) The role of the cytoskeleton and associated proteins in determination of the plant cell division plane. Plant J 75:258–269.  https://doi.org/10.1111/tpj.12177 CrossRefGoogle Scholar
  33. Sablowski R (2016) Coordination of plant cell growth and division: collective control or mutual agreement? Curr Opin Plant Biol 34:54–60.  https://doi.org/10.1016/j.pbi.2016.09.004 CrossRefGoogle Scholar
  34. Sachs J (1878) Über die Anordnung der Zellen in jüngsten Pflanzentheilen. Arb Bot Inst Würzburg 2:46–104Google Scholar
  35. Sahlin P, Jönsson H (2010) A modeling study on how cell division affects properties of epithelial tissues under isotropic growth. PLoS One 5:e11750CrossRefGoogle Scholar
  36. Sasai Y (2013) Cytosystems dynamics in self-organization of tissue architecture. Nature 493:318–326.  https://doi.org/10.1038/nature11859 CrossRefGoogle Scholar
  37. Scheres B, Di Laurenzio L, Willemsen V, Hauser MT, Janmaat K, Weisbeek P, Benfey PN (1995) Mutations affecting the radial organisation of the Arabidopsis root display specific defects throughout the embryonic axis. Development 121:53–62Google Scholar
  38. Shapiro BE, Tobin C, Mjolsness E, Meyerowitz EM (2015) Analysis of cell division patterns in the Arabidopsis shoot apical meristem. Proc Natl Acad Sci U S A 112:4815–4820.  https://doi.org/10.1073/pnas.1502588112 CrossRefGoogle Scholar
  39. Smith LG (2001) Plant cell division: building walls in the right places. Nat Rev Mol Cell Biol 2:33–39CrossRefGoogle Scholar
  40. Venverloo CJ (1990) Regulation of the plane of cell-division in vacuolated cells. 2. Wound-induced changes. Protoplasma 155:85–94CrossRefGoogle Scholar
  41. Yasuhara H, Oe Y (2011) TMBP200, a XMAP215 homologue of tobacco BY-2 cells, has an essential role in plant mitosis. Protoplasma 248:493–502.  https://doi.org/10.1007/s00709-010-0189-6 CrossRefGoogle Scholar
  42. Yoshida S, Barbier de Reuille P, Lane B, Bassel GW, Prusinkiewicz P, Smith RS, Weijers D (2014) Genetic control of plant development by overriding a genometric division rule. Dev Cell 29:75–87.  https://doi.org/10.1016/j.devcel.2014.02.002 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Biological Science, Graduate School of ScienceOsaka UniversityOsakaJapan

Personalised recommendations