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Dynamics and roles of phragmoplast microfilaments in cell plate formation during cytokinesis of tobacco BY-2 cells

  • Articles/Cell Biology
  • Published:
Chinese Science Bulletin

Abstract

The phragmoplast is a special apparatus that functions in establishing a cell plate in dividing plant cells. It is known that microfilaments (MFs) are involved in constituting phragmoplast structure, but the dynamic distribution and role of phragmoplast MFs are far from being understood. In this study, the precise structure and dynamics of MFs during the initiation and the late lateral expansion of the phragmoplast were observed by using a tobacco BY-2 cell line stably expressing the microfilament reporter construct GFP-fABD2. Three-dimensional imaging showed that the phragmoplast MFs were initiated by two populations of MFs emerging between the reconstituting daughter nuclei at anaphase, which migrated to the mid-zone and gave rise to two layers of microfilament arrays. FM4-64 stained vesicles accumulated and fused with the cell plate between the two populations of MFs. The two layers of microfilament arrays of phragmoplast with ends overlapped always surrounded the centrifugally expanding cell plate. Partial disruption of MFs at metaphase by low concentration of latrunculin B resulted in the inhibition of the cell plate consolidation and the blockage of cell plate lateral expansion, whereas high concentration of latrunculin B restrained the progression of the cell cycle. Treating the cell after the initiation of phragmoplast led to the cease of the expansion of the cell plate. Our observations provide new insights into the precise structure and dynamics of phragmoplast MFs during cytokinesis and suggest that dynamic phragmoplast MFs are important in cell plate formation.

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References

  1. Verma D P. Cytokinesis and building of the cell plate in plants. Annu Rev Plant Physiol Plant Mol Biol, 2001, 52: 751–784

    Article  Google Scholar 

  2. Jürgens G. Plant cytokinesis: fission by fusion. Trends Cell Biol, 2005, 15: 277–283

    Article  Google Scholar 

  3. Samuels A L, Giddings T HJr, Staehelin L A. Cytokinesis in tobacco BY-2 and root tip cells: A new model of cell plate formation in higher plants. J Cell Biol, 1995, 130: 1345–1357

    Article  Google Scholar 

  4. Zhang D, Wadsworth P, Hepler P K. Dynamics of microfilaments are similar, but distinct from microtubules during cytokinesis in living dividing plant cells. Cell Motil Cytoskel, 1993, 24: 151–155

    Article  Google Scholar 

  5. Jürgens G. Cytokinesis in higher plants. Annu Rev Plant Biol, 2005, 56: 281–299

    Article  Google Scholar 

  6. Kakimoto T, Shibaoka H. Cytoskeletal ultrastructure of phragmoplast-nuclei complexes isolated from cultured tobacco cells. Protoplasma, 1988, 2(suppl.): 95–103

    Google Scholar 

  7. Parke J, Miller C, Anderton B H. Higher plant myosin heavy chain identified using a monoclonal antibody. Eur J Cell Biol, 1986, 41: 9–13

    Google Scholar 

  8. Molchan T M, Valster A H, Hepler P K. Actomyosin promotes cell plate alignment and late lateral expansion in Tradescantia stamen hair cells. Planta, 2002, 214: 683–693

    Article  Google Scholar 

  9. Kakimoto T, Shibaoka H. Actin filaments and microtubules in the preprophase band and phragmoplast of tobacco cells. Protoplasma 1987, 140: 151–156

    Article  Google Scholar 

  10. Valster A, Hepler P K. Caffeine inhibition of cytokinesis: effect on the phragmoplast cytoskeleton in living Tradescantia stamen hair cells. Protoplasma, 1997, 196: 155–166

    Article  Google Scholar 

  11. Valster A H, Pierson E S, Valenta R, et al. Probing the plant actin cytoskeleton during cytokinesis and interphase by profilin microinjection. Plant Cell, 1997, 9: 1815–1824

    Article  Google Scholar 

  12. Yu M, Yuan M, Ren H. Visualization of actin cytoskeletal dynamics during the cell cycle in tobacco (Nicotiana tabacum L. cv Bright Yellow) cells. Biol Cell, 2006, 98: 295–306

    Article  Google Scholar 

  13. Kost B, Spielhofer P, Chua N H. A GFP-mouse talin fusion protein labels plant actin filaments in vivo and visualizes the actin cytoskeleton in growing pollen tubes. Plant J, 1998, 16: 393–401

    Article  Google Scholar 

  14. Sheahan M B, Staiger C J, Rose R J, et al. A green fluorescent protein fusion to actin-binding domain 2 of Arabidopsis fimbrin highlights new features of a dynamic actin cytoskeleton in live plant cells. Plant Physiol, 2004, 136: 3968–3978

    Article  Google Scholar 

  15. Voigt B, Timmers A C, Samaj J, et al. GFP-FABD2 fusion construct allows in vivo visualization of the dynamic actin cytoskeleton in all cells of Arabidopsis seedlings. Eur J Cell Biol, 2005, 84: 595–608

    Article  Google Scholar 

  16. Sano T, Higaki T, Oda Y, et al. Appearance of actin microfilament ‘etwin peaks’ in mitosis and their function in cell plate formation, as visualized in tobacco BY-2 cells expressing GFP-fimbrin. Plant J 2005; 44: 595–605

    Article  Google Scholar 

  17. Dhonukshe P, Baluska F, Schlicht M, et al. Endocytosis of cell surface material mediates cell plate formation during plant cytokinesis. Dev Cell, 2006, 10: 137–150

    Article  Google Scholar 

  18. Higaki T, Kutsuna N, Okubo E, et al. Actin microfilaments regulate vacuolar structure and dynamics: dual observation of actin filaments and vacuolar membrane in living tobacco BY-2 cells. Plant Cell Physiol, 2006, 47: 839–852

    Article  Google Scholar 

  19. Kutsuna N, Hasezawa S. Dynamic organization of vacuolar and microtubule structures during cell cycle progression in synchronized tobacco BY-2 cells. Plant Cell Physiol, 2002, 43: 965–973

    Article  Google Scholar 

  20. Cleary A L, Gunning B E S, Wasteneys G O, et al. Microtubule and F-actin dynamics at the division site in living Tradescantia stamen hair cells. J Cell Sci, 1992, 103: 977–988

    Google Scholar 

  21. Cooper J A. Effects of cytochalasin and phalloidin on actin. J Cell Biol, 1987, 105: 1473–1478

    Article  Google Scholar 

  22. Reisen D, Hanson M R. Association of six YFP-myosin XI-tail fusions with mobile plant cell organelles. BMC Plant Biol, 2007, 7: 6

    Article  Google Scholar 

  23. Esseling-Ozdoba A, Vos J W, van Lammeren A A M, et al. Synthetic lipid (DOPG) vesicles accumulate in the cell plate region but do not fuse. Plant Physiol, 2008, 147: 1699–1709

    Article  Google Scholar 

  24. Voigt B, Timmers A, Samaj J, et al. Actin-based motility of endosomes is linked to polar tip-growth of root hairs. Eur J Cell Biol, 2005, 84: 609–621

    Article  Google Scholar 

  25. Higaki T, Kutsuna N, Sano T, et al. Quantitative analysis of changes in actin microfilament contribution to cell plate development in plant cytokinesis. BMC Plant Biol, 2008, 8: 80

    Article  Google Scholar 

  26. Ingouff M, Gerald J N F, Guerin C, et al. Plant formin AtFH5 is an evolutionarily conserved actin nucleator involved in cytokinesis. Nat Cell Biol, 2005, 7: 374–380

    Article  Google Scholar 

  27. Thomas C, Hoffmann C, Dieterle M, et al. Tobacco WLIM1 is a novel F-actin binding protein involved in actin cytoskeleton remodeling. Plant Cell, 2006, 18: 2194–2206

    Article  Google Scholar 

Download references

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Correspondence to HaiYun Ren.

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Supported by National Natural Science Foundation of China (Grant Nos. 30630005, 30470176) and National Key Basic Research and Development Program of China (Grant Nos. 2006CB100100, 2007CB108700)

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Zhang, Y., Zhang, W., Baluska, F. et al. Dynamics and roles of phragmoplast microfilaments in cell plate formation during cytokinesis of tobacco BY-2 cells. Chin. Sci. Bull. 54, 2051–2061 (2009). https://doi.org/10.1007/s11434-009-0265-5

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  • DOI: https://doi.org/10.1007/s11434-009-0265-5

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