Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Cell division

Plant cell division: building walls in the right places

Key Points

ONLINE SUMMARY

  • In plant cells, the division plane is predicted before mitosis by the location of a preprophase (PPB) band of microtubules and actin filaments in the cell cortex.

  • The phragmoplast, a cytoskeletal structure that guides the formation of the new cell wall after mitosis, interacts with the cortical site formerly occupied by the preprophase band to position the new wall at that site. This interaction requires actin, and recent evidence indicates a possible role for myosins as well

  • The plane of division for many plant cells can be predicted by their shapes. Cytoskeletal filaments radiating from the nucleus to the cortex may 'read' cell shape to determine the plane of division.

  • In asymmetrically dividing cells, the plane of division is coordinated with cell polarity, which has been shown to depend on actin, the cell wall and secretion.

  • In asymmetrically dividing cells of the maize leaf epidermis, Brick1 and Pangloss 1 are required for polarization of the mother cell and two Discordia genes are required for guidance of phragmoplasts to the former PPB site.

  • The Tangled1 gene of maize is required for phragmoplast guidance in most or all leaf cells. Molecular analysis of the Tangled1 gene and protein indicates that TAN1 protein might participate in the orientation of cytoskeletal structures in dividing cells through an association with microtubules.

Abstract

Plant cells are surrounded by walls that define their shapes and fix their positions with tissues. Consequently, establishment of a plant's cellular framework during development depends largely on the positions in which new walls are formed during cytokinesis. Experiments using various approaches are now building on classical studies to shed light on the mechanisms underlying the spatial control of cytokinesis.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Effects of deformation on the plane of cell division.
Figure 2: Selection of the division plane in an elongated, highly vacuolated cell18,19,20.
Figure 3: Cytoskeletal organization in dividing plant cells.
Figure 4: Stomatal development in maize34.
Figure 5: Effects of four mutations that disrupt the normal orientation of SMC divisions in maize34.
Figure 6: Function and localization of TANGLED1 (TAN1) in dividing cells of maize leaf primordia31,41,42.

Similar content being viewed by others

References

  1. Hofmeister, W. Zusatze und Berichtigungen zu den 1851 veröffentlichen Untersuchungengen der Entwicklung höherer Kryptogamen. Jahrbucher für Wissenschaft und Botanik 3, 259–293 ( 1863).

    Google Scholar 

  2. Errera, L. Über Zellformen und Siefenblasen. Botanisches Centralblatt 34, 395–399 ( 1888).

    Google Scholar 

  3. Lintilhac, P. M. & Vesecky, T. B. Stress-induced alignment of division plane in plant tissues grown in vitro. Nature 307, 363–364 ( 1984).

    Article  Google Scholar 

  4. Lynch, T. M. & Lintilhac, P. M. Mechanical signals in plant development: a new method for single cell studies. Dev. Biol. 181, 246–256 (1997). Reports a simple and fascinating experiment showing that compression of wall-less protoplasts causes them to divide primarily in a plane parallel to the compressive force.

    Article  CAS  Google Scholar 

  5. Sinnott, E. W. & Bloch, R. Cytoplasmic behavior during division of vacuolate plant cells. Proc. Natl Acad. Sci. USA 26, 223–227 (1940).

    Article  CAS  Google Scholar 

  6. Pickett-Heaps, J. D. & Northcote, D. H. Organization of microtubules and endoplasmic reticulum during mitosis and cytokinesis in wheat meristems. J. Cell Sci. 1, 109– 120 (1966).

    CAS  PubMed  Google Scholar 

  7. Venverloo, C. J., Hovenkamp, P. H., Weeda, A. J. & Libbenga, K. R. Cell division in Nautilocalyx explants. I. Phragmosome, preprophase band and plane of division. Z. Pflanzenphysiol. 100 , 161–174 (1980).

    Article  Google Scholar 

  8. Gunning, B. E. S. in The Cytoskeleton in Plant Growth and Development (ed. Lloyd, C. W.) 229–292 (Academic Press, London, 1982).A classic review – a goldmine of information related to cytokinesis and its spatial regulation in plant cells accumulated before 1982.

    Google Scholar 

  9. Palevitz, B. A. Actin in the preprophase band of Allium cepa. J. Cell Biol. 104, 1515–1519 ( 1987).

    Article  CAS  Google Scholar 

  10. Traas, J. A. et al. An actin network is present in the cytoplasm throughout the cell cycle of carrot cells and associates with the nucleus. J. Cell Biol. 105, 387–395 (1987).

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  12. Staehelin, L. A. & Hepler, P. K. Cytokinesis in higher plants. Cell 84, 821– 824 (1996).An excellent, brief review of cytokinesis in plant cells.

    Article  CAS  Google Scholar 

  13. Otegui, M. & Staehelin, L. A. Cytokinesis in flowering plants: More than one way to divide a cell. Curr. Opin. Plant Biol. 3, 493–502 (2000). A thorough and current review of the important advances that have been made in recent years in understanding how new cell walls are formed during cytokinesis.

    Article  CAS  Google Scholar 

  14. Heese, M., Ulrike, M. & Jürgens, G. Cytokinesis in flowering plants: Cellular processes and developmental integration. Curr. Opin. Plant Biol. 1, 486–491 (1998).

    Article  CAS  Google Scholar 

  15. Smith, L. G. Divide and conquer: Cytokinesis in plant cells. Curr. Opin. Plant Biol. 2, 447–453 ( 1999).

    Article  CAS  Google Scholar 

  16. Sylvester, A. W. Division decisions and the spatial regulation of cytokinesis. Curr. Opin. Plant Biol. 3, 58–66 (2000).

    Article  CAS  Google Scholar 

  17. Goodbody, K. C., Venverloo, C. J. & Lloyd, C. W. Laser microsurgery demonstrates that cytoplasmic strands anchoring the nucleus across the vacuole of pre-mitotic plant cells are under tension. Implications for division plane alignment. Development 113, 931–939 (1991).

    Google Scholar 

  18. Flanders, D. J., Rawlins, D. J., Shaw, P. J. & Lloyd, C. W. Nucleus-associated microtubules help determine the division plane of plant epidermal cells: avoidance of four-way junctions and the role of cell geometry . J. Cell Biol. 110, 1111– 1122 (1990).

    Article  CAS  Google Scholar 

  19. Lloyd, C. W. How does the cytoskeleton read the laws of geometry in aligning the division plane of plant cells? Development (Suppl.) 1, 55–65 (1991). An interesting review summarizing a series of studies published by Clive Lloyd and his colleages during the period 1988–1991, leading to a new model for how cell shape and mechanical forces influence the choice of division plane.

    Google Scholar 

  20. Lloyd, C. W. & Traas, J. A. The role of F-actin in determining the division plane of carrot suspension cells. Drug studies. Development 102, 211–221 ( 1988).

    CAS  Google Scholar 

  21. Wick, S. M. in The Cytoskeletal Basis of Plant Growth and Form (ed. Lloyd, C. W.) 231–244 (Academic Press, London, 1991 ).A review summarizing a wealth of information regarding preprophase bands and the spatial regulation of cytokinesis.

    Google Scholar 

  22. Cho, S. -O. & Wick, S. M. Microtubule orientation during stomatal differentiation in grasses. J. Cell Sci. 92, 581–594 (1989).

    Google Scholar 

  23. Cho, S.-O. & Wick, S. M. Distribution and function of actin in the developing stomatal complex of winter rye (Secale cereale cv. Puma) . Protoplasma 157, 154– 164 (1990).

    Article  Google Scholar 

  24. Pickett-Heaps, J. D. Proprophase microtubules and stomatal differentiation: some effects of centrifugation on symmetrical and asymmetrical cell division. J. Ultrastruct. Res. 27, 24–44 ( 1969). [PubMed]

    Article  Google Scholar 

  25. Pickett-Heaps, J. D., Gunning, B. E. S., Brown, R. C., Lemmon, B. E. & Cleary, A. L. The cytoplast concept in dividing plant cells: cytoplasmic domains and the evolution of spatially organized cell division. Am. J. Bot. 86, 153– 172 (1999).

    Article  CAS  Google Scholar 

  26. Kennard, J. L. & Cleary, A. L. Pre-mitotic nuclear migration in subsidiary mother cells of Tradescantia occurs in G1 of the cell cycle and requires F-actin. Cell Motil. Cytoskel. 36, 55–67 ( 1997). [PubMed]

    Article  CAS  Google Scholar 

  27. Hyman, A. A. Centrosome movement in the early divisions of Caenorhabditis elegans: a cortical site determining centrosome position. J. Cell Biol. 109, 1185–1193 ( 1989).

    Article  CAS  Google Scholar 

  28. Knoblich, J. A. Asymmetric cell division during animal development. Nature Rev. Mol. Cell Biol. 2, 11–20 (2001).

    Article  CAS  Google Scholar 

  29. Quatrano, R. S. Separation of processes associated with differentiation of two-celled Fucus embryos. Dev. Biol. 30, 209– 312 (1973).

    Article  CAS  Google Scholar 

  30. Kropf, D. L., Kloareg, B. & Quatrano, R. S. Cell wall is required for fixation of the embryonic axis in Fucus zygotes. Science 239, 187–190 (1988).

    Article  CAS  Google Scholar 

  31. Shaw, S. L. & Quatrano, R. S. The role of targeted secretion in the establishment of cell polarity and the orientation of the division plane in Fucus zygotes. Development 122, 2623–2630 (1996).

    CAS  PubMed  Google Scholar 

  32. Vroemen, C. W., Langeveld, S., Mayer, U., Ripper, G. & Jürgens, G. Pattern formation in the Arabidopsis embryo revealed by position-specific lipid transfer protein gene expression. Plant Cell 8, 783–791 ( 1996).

    Article  CAS  Google Scholar 

  33. Steinmann, T. et al. Coordinated polar localization of auxin efflux carrier PIN1 by GNOM ARF GEF. Science 286, 316– 318 (1999).

    Article  CAS  Google Scholar 

  34. Gallagher, K. & Smith, L. G. Roles for polarity and nuclear determinants in specifying daughter cell fates following an asymmetric division in the maize leaf. Curr. Biol. 10, 1229– 1232 (2000).

    Article  CAS  Google Scholar 

  35. Ota, T. The role of cytoplasm in cytokinesis of plant cells. Cytologia 26, 428–447 (1961). A classic study, the first to show the ability of a displaced phragmoplast to find the previously established division site.

    Article  Google Scholar 

  36. Gunning, B. E. S. & Wick, S. M. Preprophase bands, phragmoplasts, and spatial control of cytokinesis. J. Cell Sci. 2, S157–S179 ( 1985).

    Article  Google Scholar 

  37. Palevitz, B. A. Division plane determination in guard mother cells of Allium: Video time-lapse analysis of nuclear movements and phragmoplast rotation in the cortex. Dev. Biol. 117, 644– 654 (1986).An early demonstration of phragmoplast re-orientation during cytokinesis ensuring the attachment of a new cell wall at the former PPB site.

    Article  Google Scholar 

  38. Cleary, A. L. & Smith, L. G. The tangled1 gene is required for spatial control of cytoskeletal arrays associated with cell division during maize leaf development. Plant Cell 10, 1875 –1888 (1998).Analysis of the maize tangled1 mutant at the level of the cytoskeleton showing the failure of most phragmoplasts to position the new cell wall at the former PPB site.

    Article  CAS  Google Scholar 

  39. Mineyuki, Y. & Gunning, B. E. S. A role for preprophase bands of microtubules in maturation of new cell walls, and a general proposal on the function of preprophase band sites in cell division in higher plants. J. Cell Sci. 97, 527–537 (1990).A classic study showing that when new cell walls are forced to attach somewhere other than the former PPB site, they fail to mature normally. This leads to the proposal that the PPB directs the deposition of cell wall maturation factors at the division site during prophase, which are transferred to the new wall if it attaches at this site.

    Google Scholar 

  40. Galatis, B., Apostolakos, P. & Katsaros, C. Experimental studies on the function of the cortical cytoplasmic zone of the preprophase microtubule band. Protoplasma 122, 11–26 ( 1984).

    Article  Google Scholar 

  41. Traas, J. A. et al. Normal differentiation patterns in plants lacking microtubular preprophase bands. Nature 375, 676– 677 (1995).Analysis of the TONNEAU/FASS mutations of Arabidopsis showing that cells divide (in a disorganized manner) without forming PPBs.

    Article  CAS  Google Scholar 

  42. Palevitz, B. A. & Hepler, P. K. The control of the plane of division during stomatal differentiation in Allium. II. Drug studies. Chromosoma 46, 327– 341 (1974).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  44. Wick, S. M. Spatial aspects of cytokinesis in plant cells. Curr. Opin. Cell Biol. 3, 253–260 ( 1991).

    Article  CAS  Google Scholar 

  45. Cleary, A. L., Gunning, B. E. S., Wasteneys, G. O. & Hepler, P. K. Microtubule and F-actin dynamics at the division site in living Tradescantia stamen hair cells. J. Cell Sci. 103, 977–988 (1992).The first description of an actin-depleted zone in the cell cortex of dividing plant cells that marks the former PPB site throughout mitosis and cytokinesis.

    CAS  Google Scholar 

  46. Liu, B. & Palevitz, B. A. Organization of cortical microfilaments in dividing root cells. Cell Motil. Cytoskeleton 23 , 252–264 (1992).

    Article  Google Scholar 

  47. Cleary, A. L. F-actin redistributions at the division site in living Tradescantia stomatal complexes as revealed by microinjection of rhodamine-phalloidin. Protoplasma 185, 152–165 (1995).

    Article  Google Scholar 

  48. Molchan, T. M., Valster, A. H., Vos, J. W. & Hepler, P. K. Actomyosin promotes cell plate alignment and late lateral expansion in plant cells. Mol. Biol. Cell 10 (Suppl.):15a (1999).

  49. Smith, L. G., Hake, S. C. & Sylvester, A. W. The tangled1 mutation alters cell division orientations throughout maize leaf development without altering leaf shape . Development 122, 481– 489 (1996).

    CAS  PubMed  Google Scholar 

  50. Smith, L. G., Gerttula, S., Han, S. & Levy, J. TANGLED1: A microtubule binding protein required for spatial control of cytokinesis in maize. J. Cell Biol.(in the press). Molecular analysis of the Tangled1 gene and protein suggesting that TAN1 protein participates in the orientation of cytoskeletal structures in dividing cells through an association with microtubules

  51. Gallagher, K. & Smith, L. G. discordia mutations specifically misorient asymmetric cell divisions during development of the maize leaf epidermis . Development 126, 4623– 4633 (1999).Analysis of two mutants that disrupt the spatial regulation of asymmetric divisions in the maize leaf epidermis by interfering with phragmoplast guidance.

    CAS  PubMed  Google Scholar 

  52. Carpita, N. C. & Gibeaut, D. M. Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant J. 3, 1–30 ( 1993).

    Article  CAS  Google Scholar 

  53. Cosgrove, D. J. Assembly and enlargement of the primary cell wall in plants. Annu. Rev. Cell Dev. Biol. 13, 171–201 (1997).

    Article  CAS  Google Scholar 

  54. Alberts, B. et al. (eds) Molecular Biology of the Cell 3rd edn 1002 (Garland, New York, 1994).

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Our research is focused on the spatial regulation of cytokinesis and cell expansion during plant development. By screening for mutations altering the regular cell patterns of the maize leaf epidermis, we have identified several genes required for one or both of these processes, many of which are described in this review.

Related links

Related links

DATABASE LINKS

GNOM

ENCYCLOPEDIA OF LIFE SCIENCES

Plant cell wall biosynthesis

Plant cell walls

Glossary

PROPHASE

An early stage of the cell cycle, during which the chromosomes become condensed in preparation for mitosis.

TRANSVACUOLAR CYTOPLASMIC STRANDS

Strands of cytoplasm passing through the vacuole that link the cytoplasm around the nucleus with the cortical cytoplasm just inside the plasma membrane.

MICROTUBULE

A hollow tube, 25 nm in diameter, formed by the lateral association of 13 protofilaments, which are themselves polymers of α- and β-tubulin subunits.

PREPROPHASE BAND (PPB)

A cytoskeletal array composed of F-actin and microtubules that is found in the cell cortex of plant cells during prophase. Its position predicts the future location of the new cell wall.

F-ACTIN

(Filamentous actin). A flexible, helical polymer of G-actin (globular actin) monomers that is 5–9 nm in diameter.

CYTOKINESIS

The division of one cell into two at the conclusion of the cell cycle.

PHRAGMOPLAST

A cytoskeletal structure composed of microtubules and actin filaments that guides the formation of a new cell wall during cytokinesis (see Fig. 3).

STOMATAL COMPLEX

A group of cells in the shoot epidermis, which functions as a regulated aperture that controls the exchange of gases and moisture between internal tissues and the air.

GUARD MOTHER CELL

A precursor cell that divides to form a pair of guard cells (see 'stomatal complex').

SUBSIDIARY MOTHER CELL

A precursor cell that divides to form at least one subsidiary cell.

SUBSIDIARY CELLS

Cells flanking the guard cells of the stomatal complex. They contribute to the regulation of stomatal opening and closing by exchanging ions with the adjacent guard cells.

GUARD CELLS

The pair of cells in the centre of a stomatal complex that flank the stomatal pore.

CYTOCHALASIN

A fungal compound that specifically interferes with actin polymerization.

ZYGOTE

A single diploid cell formed by the fusion of haploid female and male gametes.

GUANINE NUCLEOTIDE EXCHANGE FACTOR

(GEF). A protein that facilitates the exchange of GDP (guanine diphosphate) for GTP (guanine triphosphate) in the nucleotide-binding pocket of a GTP-binding protein.

ADP-RIBOSYLATION FACTOR (ARF) G PROTEIN

A GTP-binding protein that regulates the ribosylation of ADP (adenosine diphosphate).

CELL CORTEX

A thin layer of cytoplasm immediately adjacent to the inner surface of the plasma membrane.

LEAF PRIMORDIUM

A newly initiated organ that will eventually give rise to a mature leaf.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Smith, L. Plant cell division: building walls in the right places. Nat Rev Mol Cell Biol 2, 33–39 (2001). https://doi.org/10.1038/35048050

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1038/35048050

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing