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Asymmetric cell division in land plants and algae: the driving force for differentiation

Nature Reviews Molecular Cell Biology volume 12, pages 177–188 (2011)Cite this article

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A Corrigendum to this article was published on 23 March 2011

This article has been updated

Key Points

  • Asymmetric cell division is essential in many organisms to generate cell diversity and tissue patterns and to maintain pools of stem cells. In plants and multicellular algae, asymmetric cell division is of particular importance, as their post-embryonic growth is based on de novo formation of cell types, tissues and even entirely new organs.

  • Daughter cells, which can be initially equivalent or different in size and/or molecular composition, can achieve different cell fates through intrinsic or extrinsic factors that convey positional information. These seemingly distinct mechanisms can rarely be separated, and it is becoming clear that every asymmetric cell division depends on both extrinsic and intrinsic factors simultaneously.

  • Asymmetric cell division in plants involves numerous steps: specification of a subset of cells that will undergo asymmetric cell division; cellular events (such as establishment of polarity, polar localization of proteins, establishment of gradients, correct positioning of the nucleus, polar accumulation of the cytoplasm and formation of the preprophase band, spindle and cell plate); and the asymmetrical distribution and expression of cell fate determinants. Together, these control the identity and future development of both daughter cells into a differentiated tissue or new organ. However, not all steps are necessarily present in every asymmetric cell division process.

  • In animals, the cell cycle has been linked to asymmetric localization of cell fate determinants and, consistently, the regulation of asymmetric cell division needs to be precisely coordinated with cell cycle progression in plants as well.

  • Various developmental processes require asymmetric cell division and use similar, or even the same, mechanisms and/or conserved molecular players.

Abstract

Asymmetric cell division generates two cells with different fates and has an important role in plant development. It produces distinct cell types and new organs, and maintains stem cell niches. To handle the constraints of having immobile cells, plants possess numerous unique features to obtain asymmetry, such as specific regulators of intrinsic polarity. Although several components have not yet been identified, new findings, together with knowledge from different developmental systems, now allow us to take an important step towards a mechanistic overview of asymmetric cell division in plants and algae. Strikingly, several key regulators are used for different developmental processes, and common mechanisms can be recognized.

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Figure 1: Main mechanisms for establishment of asymmetric cell identities in plants and algae.
Figure 2: Typical asymmetric cell divisions in plants.
Figure 3: Key events before asymmetric cell divisions.
Figure 4: Asymmetrically expressed determinants after asymmetric cell division, and the role of cell cycle activity.
Figure 5: Common regulatory mechanisms during asymmetric cell division.

Change history

  • 23 March 2011

    On page 183 of this article there was a mistake in the sentence "These include the genes encoding the transcription factors PROTODERMAL FACTOR 2 (PDF2)18,85 and ARABIDOPSIS THALIANA MERISTEM LAYER 1 (ATML1)18,86 and the LRR receptor-like kinase ARABIDOPSIS CRINKLY 4 (ACR4)87,88." ACR4 is not an LRR family protein. This has been corrected online.

References

  1. Abrash, E. B. & Bergmann, D. C. Asymmetric cell divisions: a view from plant development. Dev. Cell 16, 783–796 (2009).

    Article  CAS  PubMed  Google Scholar 

  2. Horvitz, H. R. & Herskowitz, I. Mechanisms of asymmetric cell division: two Bs or not two Bs, that is the question. Cell 68, 237–255 (1992).

    Article  CAS  PubMed  Google Scholar 

  3. Knoblich, J. A. Mechanisms of asymmetric stem cell division. Cell 132, 583–597 (2008).

    Article  CAS  PubMed  Google Scholar 

  4. Scheres, B. & Benfey, P. N. Asymmetric cell division in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50, 505–537 (1999).

    Article  CAS  PubMed  Google Scholar 

  5. Schlereth, A. et al. MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor. Nature 464, 913–916 (2010).

    Article  CAS  PubMed  Google Scholar 

  6. Weijers, D. et al. Auxin triggers transient local signaling for cell specification in Arabidopsis embryogenesis. Dev. Cell 10, 265–270 (2006).

    Article  CAS  PubMed  Google Scholar 

  7. Dong, J., MacAlister, C. A. & Bergmann, D. C. BASL controls asymmetric cell division in Arabidopsis. Cell 137, 1320–1330 (2009). Describes a new regulator of asymmetric cell divisions that seems to be unique to plants.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Berger, F. & Brownlee, C. Ratio confocal imaging of free cytoplasmic calcium gradients in polarising and polarised Fucus zygotes. Zygote 1, 9–15 (1993).

    Article  CAS  PubMed  Google Scholar 

  9. Bouget, F. Y., Gerttula, S., Shaw, S. L. & Quatrano, R. S. Localization of actin mRNA during the establishment of cell polarity and early cell divisions in Fucus embryos. Plant Cell 8, 189–201 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Pu, R. & Robinson, K. R. Cytoplasmic calcium gradients and calmodulin in the early development of the fucoid alga Pelvetia compressa. J. Cell Sci. 111, 3197–3207 (1998).

    Article  CAS  PubMed  Google Scholar 

  11. De Rybel, B. et al. A novel aux/IAA28 signaling cascade activates GATA23-dependent specification of lateral root founder cell identity. Curr. Biol. 20, 1697–1706 (2010).

    Article  CAS  PubMed  Google Scholar 

  12. Mansfield, S. G. & Briarty, L. G. Early embryogenesis in Arabidopsis thaliana: II. The developing embryo. Can. J. Bot. 69, 461–476 (1991).

    Article  Google Scholar 

  13. Smith, L. G. Plant cell division: building walls in the right places. Nature Rev. Mol. Cell Biol. 2, 33–39 (2001).

    Article  CAS  Google Scholar 

  14. Borg, M., Brownfield, L. & Twell, D. Male gametophyte development: a molecular perspective. J. Exp. Bot. 60, 1465–1478 (2009).

    Article  CAS  PubMed  Google Scholar 

  15. Bisgrove, S. R. & Kropf, D. L. Asymmetric cell divisions: zygotes of fucoid algae as a model system. Plant Cell Monographs 9, 323–341 (2008).

    Article  Google Scholar 

  16. Mayer, U., Buttner, G. & Jürgens, G. Apical–basal pattern formation in the Arabidopsis embryo: studies on the role of the gnom gene. Development 117, 149–162 (1993).

    Article  Google Scholar 

  17. De Smet, I., Lau, S., Mayer, U. & Jürgens, G. Embryogenesis — the humble beginnings of plant life. Plant J. 61, 959–970 (2010).

    Article  CAS  PubMed  Google Scholar 

  18. Lau, S. et al. Cell–cell communication in Arabidopsis early embryogenesis. Eur. J. Cell Biol. 89, 225–230 (2010).

    Article  CAS  PubMed  Google Scholar 

  19. De Smet, I. et al. Receptor-like kinase ACR4 restricts formative cell divisions in the Arabidopsis root. Science 322, 594–597 (2008). Describes the first receptor-like kinase that is involved in the control of formative divisions in the root.

    Article  CAS  PubMed  Google Scholar 

  20. Peterson, K. M., Rychel, A. L. & Torii, K. U. Out of the mouths of plants: the molecular basis of the evolution and diversity of stomatal development. Plant Cell 22, 296–306 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Malamy, J. E. & Benfey, P. N. Organization and cell differentiation in lateral roots of Arabidopsis thaliana. Development 124, 33–44 (1997).

    Article  CAS  PubMed  Google Scholar 

  22. Willemsen, V. et al. The NAC domain transcription factors FEZ and SOMBRERO control the orientation of cell division plane in Arabidopsis root stem cells. Dev. Cell 15, 913–922 (2008).

    Article  CAS  PubMed  Google Scholar 

  23. Bonke, M., Thitamadee, S., Mahonen, A. P., Hauser, M. T. & Helariutta, Y. APL regulates vascular tissue identity in Arabidopsis. Nature 426, 181–186 (2003).

    Article  CAS  PubMed  Google Scholar 

  24. Mahonen, A. P. et al. A novel two-component hybrid molecule regulates vascular morphogenesis of the Arabidopsis root. Genes Dev. 14, 2938–2943 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Elo, A., Immanen, J., Nieminen, K. & Helariutta, Y. Stem cell function during plant vascular development. Semin. Cell Dev. Biol. 20, 1097–1106 (2009).

    Article  CAS  PubMed  Google Scholar 

  26. Carlsbecker, A. et al. Cell signalling by microRNA165/6 directs gene dose-dependent root cell fate. Nature 465, 316–321 (2010). Describes how vascular patterning occurs through crosstalk between the vascular cylinder and the surrounding endodermis, mediated by cell-to-cell movement of the SHR transcription factor in one direction and microRNAs in the other.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Hord, C. L., Chen, C., Deyoung, B. J., Clark, S. E. & Ma, H. The BAM1/BAM2 receptor-like kinases are important regulators of Arabidopsis early anther development. Plant Cell 18, 1667–1680 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Wilson, Z. A. & Zhang, D. B. From Arabidopsis to rice: pathways in pollen development. J. Exp. Bot. 60, 1479–1492 (2009).

    Article  CAS  PubMed  Google Scholar 

  29. De Smet, I., Voss, U., Jurgens, G. & Beeckman, T. Receptor-like kinases shape the plant. Nature Cell Biol. 11, 1166–1173 (2009).

    Article  CAS  PubMed  Google Scholar 

  30. Yang, W. C., Ye, D., Xu, J. & Sundaresan, V. The SPOROCYTELESS gene of Arabidopsis is required for initiation of sporogenesis and encodes a novel nuclear protein. Genes Dev. 13, 2108–2117 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Prochiantz, A. & Joliot, A. Can transcription factors function as cell–cell signalling molecules? Nature Rev. Mol. Cell Biol. 4, 814–819 (2003).

    Article  CAS  Google Scholar 

  32. Gallagher, K. L. & Benfey, P. N. Not just another hole in the wall: understanding intercellular protein trafficking. Genes Dev. 19, 189–195 (2005).

    Article  CAS  PubMed  Google Scholar 

  33. Guseman, J. M. et al. Dysregulation of cell-to-cell connectivity and stomatal patterning by loss-of-function mutation in Arabidopsis CHORUS (GLUCAN SYNTHASE-LIKE 8). Development 137, 1731–1741 (2010).

    Article  CAS  PubMed  Google Scholar 

  34. Nakajima, K., Sena, G., Nawy, T. & Benfey, P. N. Intercellular movement of the putative transcription factor SHR in root patterning. Nature 413, 307–311 (2001). This paper and reference 5 describe mobile transcription factors, which are involved in root establishment and patterning.

    Article  CAS  PubMed  Google Scholar 

  35. Cui, H. et al. An evolutionarily conserved mechanism delimiting SHR movement defines a single layer of endodermis in plants. Science 316, 421–425 (2007).

    Article  CAS  PubMed  Google Scholar 

  36. Gallagher, K. L. & Benfey, P. N. Both the conserved GRAS domain and nuclear localization are required for SHORT-ROOT movement. Plant J. 57, 785–797 (2009).

    Article  CAS  PubMed  Google Scholar 

  37. De Smet, I. et al. Auxin-dependent regulation of lateral root positioning in the basal meristem of Arabidopsis. Development 134, 681–690 (2007).

    Article  CAS  PubMed  Google Scholar 

  38. Moreno-Risueno, M. A. et al. Oscillating gene expression determines competence for periodic Arabidopsis root branching. Science 329, 1306–1311 (2010). Reveals sets of genes oscillating in opposite phases at the root tip that are involved in founder cell production and root bending, a mechanism resembling molecular clock-driven activities in animals.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Richter, G. L., Monshausen, G. B., Krol, A. & Gilroy, S. Mechanical stimuli modulate lateral root organogenesis. Plant Physiol. 151, 1855–1866 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Hunt, L. & Gray, J. E. The signaling peptide EPF2 controls asymmetric cell divisions during stomatal development. Curr. Biol. 19, 864–869 (2009).

    Article  CAS  PubMed  Google Scholar 

  41. Lampard, G. R., Lukowitz, W., Ellis, B. E. & Bergmann, D. C. Novel and expanded roles for MAPK signaling in Arabidopsis stomatal cell fate revealed by cell type-specific manipulations. Plant Cell 21, 3506–3517 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Lampard, G. R., Macalister, C. A. & Bergmann, D. C. Arabidopsis stomatal initiation is controlled by MAPK-mediated regulation of the bHLH SPEECHLESS. Science 322, 1113–1116 (2008). Couples a general MAPK signalling cascade to particular transcription factor activity to generate a specific output.

    Article  CAS  PubMed  Google Scholar 

  43. Sugano, S. S. et al. Stomagen positively regulates stomatal density in Arabidopsis. Nature 463, 241–244 (2010). Provides evidence of a mesophyll-derived positive regulator of stomatal density.

    Article  CAS  PubMed  Google Scholar 

  44. Shpak, E. D., McAbee, J. M., Pillitteri, L. J. & Torii, K. U. Stomatal patterning and differentiation by synergistic interactions of receptor kinases. Science 309, 290–293 (2005).

    Article  CAS  PubMed  Google Scholar 

  45. Grunewald, W. & Friml, J. The march of the PINs: developmental plasticity by dynamic polar targeting in plant cells. EMBO J. 29, 2700–2714 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Neumuller, R. A. & Knoblich, J. A. Dividing cellular asymmetry: asymmetric cell division and its implications for stem cells and cancer. Genes Dev. 23, 2675–2699 (2009).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  47. Geldner, N. et al. Partial loss-of-function alleles reveal a role for GNOM in auxin transport-related, post-embryonic development of Arabidopsis. Development 131, 389–400 (2004).

    Article  CAS  PubMed  Google Scholar 

  48. Cartwright, H. N., Humphries, J. A. & Smith, L. G. PAN1: a receptor-like protein that promotes polarization of an asymmetric cell division in maize. Science 323, 649–651 (2009). Shows that a receptor-like kinase with an inactive kinase domain is involved in transmitting an extrinsic signal to polarize asymmetric cell divisions in maize stomata development.

    Article  CAS  PubMed  Google Scholar 

  49. Brownlee, C., Bouget, F. Y. & Corellou, F. Choosing sides: establishment of polarity in zygotes of fucoid algae. Semin. Cell Dev. Biol. 12, 345–351 (2001).

    Article  CAS  PubMed  Google Scholar 

  50. Shaw, S. L. & Quatrano, R. S. Polar localization of a dihydropyridine receptor on living Fucus zygotes. J. Cell Sci. 109, 335–342 (1996).

    Article  CAS  PubMed  Google Scholar 

  51. Bothwell, J. H., Kisielewska, J., Genner, M. J., McAinsh, M. R. & Brownlee, C. Ca2+ signals coordinate zygotic polarization and cell cycle progression in the brown alga Fucus serratus. Development 135, 2173–2181 (2008).

    Article  CAS  PubMed  Google Scholar 

  52. Love, J., Brownlee, C. & Trewavas, A. J. Ca2+ and calmodulin dynamics during photopolarization in Fucus serratus zygotes. Plant Physiol. 115, 249–261 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Sun, H., Basu, S., Brady, S. R., Luciano, R. L. & Muday, G. K. Interactions between auxin transport and the actin cytoskeleton in developmental polarity of Fucus distichus embryos in response to light and gravity. Plant Physiol. 135, 266–278 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Kropf, D. L., Bisgrove, S. R. & Hable, W. E. Establishing a growth axis in fucoid algae. Trends Plant Sci. 4, 490–494 (1999).

    Article  CAS  PubMed  Google Scholar 

  55. Panteris, E., Apostolakos, P. & Galatis, B. Cytoskeletal asymmetry in Zea mays subsidiary cell mother cells: a monopolar prophase microtubule half-spindle anchors the nucleus to its polar position. Cell Motil. Cytoskeleton 63, 696–709 (2006).

    Article  CAS  PubMed  Google Scholar 

  56. Twell, D., Park, S. K. & Lalanne, E. Asymmetric division and cell-fate determination in developing pollen. Trends Plant Sci. 3, 305–310 (1998).

    Article  Google Scholar 

  57. Edwards, E. S. & Roux, S. J. Influence of gravity and light on the developmental polarity of Ceratopteris richardii fern spores. Planta 205, 553–560 (1998).

    Article  CAS  PubMed  Google Scholar 

  58. Vogelmann, T. C., Bassel, A. R. & Miller, J. H. Effects of microtubule-inhibitors on nuclear migration and rhizoid differentiation in germinating fern spores (Onoclea sensibilis). Protoplasma 109, 295–316 (1981).

    Article  CAS  Google Scholar 

  59. Srilunchang, K. O., Krohn, N. G. & Dresselhaus, T. DiSUMO-like DSUL is required for nuclei positioning, cell specification and viability during female gametophyte maturation in maize. Development 137, 333–345 (2010).

    Article  CAS  PubMed  Google Scholar 

  60. Oh, S. A., Pal, M. D., Park, S. K., Johnson, J. A. & Twell, D. The tobacco MAP215/Dis1-family protein TMBP200 is required for the functional organization of microtubule arrays during male germline establishment. J. Exp. Bot. 61, 969–981 (2010).

    Article  CAS  PubMed  Google Scholar 

  61. Park, S. K., Howden, R. & Twell, D. The Arabidopsis thaliana gametophytic mutation gemini pollen1 disrupts microspore polarity, division asymmetry and pollen cell fate. Development 125, 3789–3799 (1998).

    Article  CAS  PubMed  Google Scholar 

  62. Müller, S., Wright, A. J. & Smith, L. G. Division plane control in plants: new players in the band. Trends Cell Biol. 19, 180–188 (2009).

    Article  PubMed  CAS  Google Scholar 

  63. Van Damme, D. Division plane determination during plant somatic cytokinesis. Curr. Opin. Plant Biol. 12, 745–751 (2009).

    Article  CAS  PubMed  Google Scholar 

  64. Van Damme, D., Vanstraelen, M. & Geelen, D. Cortical division zone establishment in plant cells. Trends Plant Sci. 12, 458–464 (2007).

    Article  CAS  PubMed  Google Scholar 

  65. Gallagher, K. & Smith, L. G. discordia mutations specifically misorient asymmetric cell divisions during development of the maize leaf epidermis. Development 126, 4623–4633 (1999).

    Article  CAS  PubMed  Google Scholar 

  66. Wright, A. J., Gallagher, K. & Smith, L. G. discordia1 and alternative discordia1 function redundantly at the cortical division site to promote preprophase band formation and orient division planes in maize. Plant Cell 21, 234–247 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Torres-Ruiz, R. A. & Jurgens, G. Mutations in the FASS gene uncouple pattern formation and morphogenesis in Arabidopsis development. Development 120, 2967–2978 (1994).

    Article  CAS  PubMed  Google Scholar 

  68. Harrison, C. J., Roeder, A. H., Meyerowitz, E. M. & Langdale, J. A. Local cues and asymmetric cell divisions underpin body plan transitions in the moss Physcomitrella patens. Curr. Biol. 19, 461–471 (2009).

    Article  CAS  PubMed  Google Scholar 

  69. Gönczy, P. Mechanisms of asymmetric cell division: flies and worms pave the way. Nature Rev. Mol. Cell Biol. 9, 355–366 (2008).

    Article  CAS  Google Scholar 

  70. Kirk, D. L. & Nishii, I. Volvox carteri as a model for studying the genetic and cytological control of morphogenesis. Dev. Growth Differ. 43, 621–631 (2001).

    Article  CAS  PubMed  Google Scholar 

  71. Borges, F. et al. Comparative transcriptomics of Arabidopsis sperm cells. Plant Physiol. 148, 1168–1181 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Engel, M. L., Holmes-Davis, R. & McCormick, S. Green sperm. Identification of male gamete promoters in Arabidopsis. Plant Physiol. 138, 2124–2133 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Mori, T., Kuroiwa, H., Higashiyama, T. & Kuroiwa, T. GENERATIVE CELL SPECIFIC 1 is essential for angiosperm fertilization. Nature Cell Biol. 8, 64–71 (2006).

    Article  CAS  PubMed  Google Scholar 

  74. Rotman, N. et al. A novel class of MYB factors controls sperm-cell formation in plants. Curr. Biol. 15, 244–248 (2005).

    Article  CAS  PubMed  Google Scholar 

  75. Xu, H., Swoboda, I., Bhalla, P. L. & Singh, M. B. Male gametic cell-specific gene expression in flowering plants. Proc. Natl Acad. Sci. USA 96, 2554–2558 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Breuninger, H., Rikirsch, E., Hermann, M., Ueda, M. & Laux, T. Differential expression of WOX genes mediates apical-basal axis formation in the Arabidopsis embryo. Dev. Cell 14, 867–876 (2008).

    Article  CAS  PubMed  Google Scholar 

  77. Haecker, A. et al. Expression dynamics of WOX genes mark cell fate decisions during early embryonic patterning in Arabidopsis thaliana. Development 131, 657–668 (2004).

    Article  CAS  PubMed  Google Scholar 

  78. Hamann, T., Benkova, E., Baurle, I., Kientz, M. & Jürgens, G. The Arabidopsis BODENLOS gene encodes an auxin response protein inhibiting MONOPTEROS-mediated embryo patterning. Genes Dev. 16, 1610–1615 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Hamann, T., Mayer, U. & Jürgens, G. The auxin-insensitive bodenlos mutation affects primary root formation and apical-basal patterning in the Arabidopsis embryo. Development 126, 1387–1395 (1999).

    Article  CAS  PubMed  Google Scholar 

  80. Hardtke, C. S. & Berleth, T. The Arabidopsis gene MONOPTEROS encodes a transcription factor mediating embryo axis formation and vascular development. EMBO J. 17, 1405–1411 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Friml, J. et al. Efflux-dependent auxin gradients establish the apical–basal axis of Arabidopsis. Nature 426, 147–153 (2003).

    Article  CAS  PubMed  Google Scholar 

  82. Lukowitz, W., Roeder, A., Parmenter, D. & Somerville, C. A MAPKK kinase gene regulates extra-embryonic cell fate in Arabidopsis. Cell 116, 109–119 (2004).

    Article  CAS  PubMed  Google Scholar 

  83. Wang, H., Ngwenyama, N., Liu, Y., Walker, J. C. & Zhang, S. Stomatal development and patterning are regulated by environmentally responsive mitogen-activated protein kinases in Arabidopsis. Plant Cell 19, 63–73 (2007).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  84. Benkova, E. et al. Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115, 591–602 (2003).

    Article  CAS  PubMed  Google Scholar 

  85. Abe, M., Katsumata, H., Komeda, Y. & Takahashi, T. Regulation of shoot epidermal cell differentiation by a pair of homeodomain proteins in Arabidopsis. Development 130, 635–643 (2003).

    Article  CAS  PubMed  Google Scholar 

  86. Takada, S. & Jürgens, G. Transcriptional regulation of epidermal cell fate in the Arabidopsis embryo. Development 134, 1141–1150 (2007).

    Article  CAS  PubMed  Google Scholar 

  87. Gifford, M. L., Dean, S. & Ingram, G. C. The Arabidopsis ACR4 gene plays a role in cell layer organisation during ovule integument and sepal margin development. Development 130, 4249–4258 (2003).

    Article  CAS  PubMed  Google Scholar 

  88. Tanaka, H. et al. ACR4, a putative receptor kinase gene of Arabidopsis thaliana, that is expressed in the outer cell layers of embryos and plants, is involved in proper embryogenesis. Plant Cell Physiol. 43, 419–428 (2002).

    Article  CAS  PubMed  Google Scholar 

  89. Lynn, K. et al. The PINHEAD/ZWILLE gene acts pleiotropically in Arabidopsis development and has overlapping functions with the ARGONAUTE1 gene. Development 126, 469–481 (1999).

    Article  CAS  PubMed  Google Scholar 

  90. Wysocka-Diller, J. W., Helariutta, Y., Fukaki, H., Malamy, J. E. & Benfey, P. N. Molecular analysis of SCARECROW function reveals a radial patterning mechanism common to root and shoot. Development 127, 595–603 (2000).

    Article  CAS  PubMed  Google Scholar 

  91. Sarkar, A. K. et al. Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature 446, 811–814 (2007).

    Article  CAS  PubMed  Google Scholar 

  92. Hara, K. et al. Epidermal cell density is autoregulated via a secretory peptide, EPIDERMAL PATTERNING FACTOR 2 in Arabidopsis leaves. Plant Cell Physiol. 50, 1019–1031 (2009).

    Article  CAS  PubMed  Google Scholar 

  93. Etchells, J. P. & Turner, S. R. The PXY-CLE41 receptor ligand pair defines a multifunctional pathway that controls the rate and orientation of vascular cell division. Development 137, 767–774 (2010).

    Article  CAS  PubMed  Google Scholar 

  94. Fisher, K. & Turner, S. PXY, a receptor-like kinase essential for maintaining polarity during plant vascular-tissue development. Curr. Biol. 17, 1061–1066 (2007).

    Article  CAS  PubMed  Google Scholar 

  95. Hirakawa, Y. et al. Non-cell-autonomous control of vascular stem cell fate by a CLE peptide/receptor system. Proc. Natl Acad. Sci. USA 105, 15208–15213 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Yoda, A., Kouike, H., Okano, H. & Sawa, H. Components of the transcriptional Mediator complex are required for asymmetric cell division in C. elegans. Development 132, 1885–1893 (2005).

    Article  CAS  PubMed  Google Scholar 

  97. Gillmor, C. S. et al. The MED12–MED13 module of Mediator regulates the timing of embryo patterning in Arabidopsis. Development 137, 113–122 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Eady, C., Lindsey, K. & Twell, D. The significance of microspore division and division symmetry for vegetative cell-specific transcription and generative cell differentiation. Plant Cell 7, 65–74 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Haerizadeh, F., Singh, M. B. & Bhalla, P. L. Transcriptional repression distinguishes somatic from germ cell lineages in a plant. Science 313, 496–499 (2006).

    Article  CAS  PubMed  Google Scholar 

  100. Isshiki, T., Pearson, B., Holbrook, S. & Doe, C. Q. Drosophila neuroblasts sequentially express transcription factors which specify the temporal identity of their neuronal progeny. Cell 106, 511–521 (2001).

    Article  CAS  PubMed  Google Scholar 

  101. Prokopenko, S. N. & Chia, W. When timing is everything: role of cell cycle regulation in asymmetric division. Semin. Cell Dev. Biol. 16, 423–437 (2005).

    Article  CAS  PubMed  Google Scholar 

  102. De Smet, I. et al. Bimodular auxin response controls organogenesis in Arabidopsis. Proc. Natl Acad. Sci. USA 107, 2705–2710 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. MacAlister, C. A., Ohashi-Ito, K. & Bergmann, D. C. Transcription factor control of asymmetric cell divisions that establish the stomatal lineage. Nature 445, 537–540 (2007).

    Article  CAS  PubMed  Google Scholar 

  104. Pillitteri, L. J., Sloan, D. B., Bogenschutz, N. L. & Torii, K. U. Termination of asymmetric cell division and differentiation of stomata. Nature 445, 501–505 (2007).

    Article  CAS  PubMed  Google Scholar 

  105. Kawashima, T. & Goldberg, R. B. The suspensor: not just suspending the embryo. Trends Plant Sci. 15, 23–30 (2010).

    Article  CAS  PubMed  Google Scholar 

  106. Kawashima, T. et al. Identification of cis-regulatory sequences that activate transcription in the suspensor of plant embryos. Proc. Natl Acad. Sci. USA 106, 3627–3632 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Weterings, K. et al. Regional localization of suspensor mRNAs during early embryo development. Plant Cell 13, 2409–2425 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Du, T. G., Schmid, M. & Jansen, R. P. Why cells move messages: the biological functions of mRNA localization. Semin. Cell Dev. Biol. 18, 171–177 (2007).

    Article  CAS  PubMed  Google Scholar 

  109. Wilhelm, J. E. & Vale, R. D. RNA on the move: the mRNA localization pathway. J. Cell Biol. 123, 269–274 (1993).

    Article  CAS  PubMed  Google Scholar 

  110. Jansen, R. P. mRNA localization: message on the move. Nature Rev. Mol. Cell Biol. 2, 247–256 (2001).

    Article  CAS  Google Scholar 

  111. Bayer, M. et al. Paternal control of embryonic patterning in Arabidopsis thaliana. Science 323, 1485–1488 (2009). Proposes that SSP produced from paternal transcripts triggers zygotic YDA activity upon fertilization, providing an essential temporal cue for the regulation of the first asymmetric cell division of the zygote.

    Article  CAS  PubMed  Google Scholar 

  112. Stahl, Y., Wink, R. H., Ingram, G. C. & Simon, R. A signaling module controlling the stem cell niche in Arabidopsis root meristems. Curr. Biol. 19, 909–914 (2009).

    Article  CAS  PubMed  Google Scholar 

  113. Kieffer, M., Neve, J. & Kepinski, S. Defining auxin response contexts in plant development. Curr. Opin. Plant Biol. 13, 12–20 (2010).

    Article  CAS  PubMed  Google Scholar 

  114. Levesque, M. P. et al. Whole-genome analysis of the SHORT-ROOT developmental pathway in Arabidopsis. PLoS Biol. 4, e143 (2006).

    Article  PubMed  PubMed Central  Google Scholar 

  115. Mylona, P., Linstead, P., Martienssen, R. & Dolan, L. SCHIZORIZA controls an asymmetric cell division and restricts epidermal identity in the Arabidopsis root. Development 129, 4327–4334 (2002).

    Article  CAS  PubMed  Google Scholar 

  116. Pernas, M., Ryan, E. & Dolan, L. SCHIZORIZA controls tissue system complexity in plants. Curr. Biol. 20, 818–823 (2010).

    Article  CAS  PubMed  Google Scholar 

  117. ten Hove, C. A. et al. SCHIZORIZA encodes a nuclear factor regulating asymmetry of stem cell divisions in the Arabidopsis root. Curr. Biol. 20, 452–457 (2010).

    Article  CAS  PubMed  Google Scholar 

  118. Welch, D. et al. Arabidopsis JACKDAW and MAGPIE zinc finger proteins delimit asymmetric cell division and stabilize tissue boundaries by restricting SHORT-ROOT action. Genes Dev. 21, 2196–2204 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Tio, M., Udolph, G., Yang, X. & Chia, W. cdc2 links the Drosophila cell cycle and asymmetric division machineries. Nature 409, 1063–1067 (2001).

    Article  CAS  PubMed  Google Scholar 

  120. Zhong, W. Timing cell-fate determination during asymmetric cell divisions. Curr. Opin. Neurobiol. 18, 472–478 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Hemerly, A. S., Ferreira, P. C., Van Montagu, M., Engler, G. & Inze, D. Cell division events are essential for embryo patterning and morphogenesis: studies on dominant-negative cdc2aAt mutants of Arabidopsis. Plant J. 23, 123–130 (2000).

    Article  CAS  PubMed  Google Scholar 

  122. Iwakawa, H., Shinmyo, A. & Sekine, M. Arabidopsis CDKA;1, a cdc2 homologue, controls proliferation of generative cells in male gametogenesis. Plant J. 45, 819–831 (2006).

    Article  CAS  PubMed  Google Scholar 

  123. Brownfield, L. et al. A plant germline-specific integrator of sperm specification and cell cycle progression. PLoS Genet. 5, e1000430 (2009).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  124. Kim, H. J. et al. Control of plant germline proliferation by SCFFBL17 degradation of cell cycle inhibitors. Nature 455, 1134–1137 (2008).

    Article  CAS  PubMed  Google Scholar 

  125. Oh, S. A., Park, K. S., Twell, D. & Park, S. K. The SIDECAR POLLEN gene encodes a microspore-specific LOB/AS2 domain protein required for the correct timing and orientation of asymmetric cell division. Plant J. 64, 839–850 (2010).

    Article  CAS  PubMed  Google Scholar 

  126. Sozzani, R. et al. Spatiotemporal regulation of cell-cycle genes by SHORTROOT links patterning and growth. Nature 66, 128–132 (2010). Provides evidence for a direct link among the developmental regulators SHR and SCR, the cell cycle machinery and formative cell divisions.

    Article  CAS  Google Scholar 

  127. Wildwater, M. et al. The RETINOBLASTOMA-RELATED gene regulates stem cell maintenance in Arabidopsis roots. Cell 123, 1337–1349 (2005).

    Article  CAS  PubMed  Google Scholar 

  128. Himanen, K. et al. Auxin-mediated cell cycle activation during early lateral root initiation. Plant Cell 14, 2339–2351 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Vanneste, S. et al. Cell cycle progression in the pericycle is not sufficient for SOLITARY ROOT/IAA14-mediated lateral root initiation in Arabidopsis thaliana. Plant Cell 17, 3035–3050 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Borghi, L. et al. Arabidopsis RETINOBLASTOMA-RELATED is required for stem cell maintenance, cell differentiation, and lateral organ production. Plant Cell 22, 1792–1811 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. Zhang, H. et al. ABA promotes quiescence of the quiescent centre and suppresses stem cell differentiation in the Arabidopsis primary root meristem. Plant J. 64, 764–774 (2010).

    Article  CAS  PubMed  Google Scholar 

  132. Bergmann, D. C., Lukowitz, W. & Somerville, C. R. Stomatal development and pattern controlled by a MAPKK kinase. Science 304, 1494–1497 (2004).

    Article  CAS  PubMed  Google Scholar 

  133. Vanneste, S. & Friml, J. Auxin: a trigger for change in plant development. Cell 136, 1005–1016 (2009).

    Article  CAS  PubMed  Google Scholar 

  134. Laskowski, M. et al. Root system architecture from coupling cell shape to auxin transport. PLoS Biol. 6, e307 (2008).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  135. Abrash, E. B. & Bergmann, D. C. Regional specification of stomatal production by the putative ligand CHALLAH. Development 137, 447–455 (2010).

    Article  CAS  PubMed  Google Scholar 

  136. Scheres, B. Stem-cell niches: nursery rhymes across kingdoms. Nature Rev. Mol. Cell Biol. 8, 345–354 (2007).

    Article  CAS  Google Scholar 

  137. Dinneny, J. R. & Benfey, P. N. Plant stem cell niches: standing the test of time. Cell 132, 553–557 (2008).

    Article  CAS  PubMed  Google Scholar 

  138. Reddy, G. V. Live-imaging stem-cell homeostasis in the Arabidopsis shoot apex. Curr. Opin. Plant Biol. 11, 88–93 (2008).

    Article  CAS  PubMed  Google Scholar 

  139. Suzuki, T. et al. A novel Arabidopsis gene TONSOKU is required for proper cell arrangement in root and shoot apical meristems. Plant J. 38, 673–684 (2004).

    Article  CAS  PubMed  Google Scholar 

  140. Clevers, H. Stem cells, asymmetric division and cancer. Nature Genet. 37, 1027–1028 (2005).

    Article  CAS  PubMed  Google Scholar 

  141. Ohashi-Ito, K. & Bergmann, D. C. Arabidopsis FAMA controls the final proliferation/differentiation switch during stomatal development. Plant Cell 18, 2493–2505 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  142. Tajbakhsh, S., Rocheteau, P. & Le Roux, I. Asymmetric cell divisions and asymmetric cell fates. Annu. Rev. Cell Dev. Biol. 25, 671–699 (2009).

    Article  CAS  PubMed  Google Scholar 

  143. Lau, S., Jürgens, G. & De Smet, I. The evolving complexity of the auxin pathway. Plant Cell 20, 1738–1746 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  144. Lau, S., Shao, N., Bock, R., Jürgens, G. & De Smet, I. Auxin signaling in algal lineages: fact or myth? Trends Plant Sci. 14, 182–188 (2009).

    Article  CAS  PubMed  Google Scholar 

  145. De Smet, I. et al. Unraveling the evolution of auxin signaling. Plant Physiol. 155, 209–221 (2011).

    Article  CAS  PubMed  Google Scholar 

  146. Le Bail, A. et al. Auxin metabolism and function in the multicellular brown alga Ectocarpus siliculosus. Plant Physiol. 153, 128–144 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  147. Spinner, L. et al. The function of TONNEAU1 in moss reveals ancient mechanisms of division plane specification and cell elongation in land plants. Development 137, 2733–2742 (2010).

    Article  CAS  PubMed  Google Scholar 

  148. 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).

    Article  CAS  PubMed  Google Scholar 

  149. Grunewald, W., Parizot, B., Inzé, D., Gheysen, G. & Beeckman, T. Developmental biology of roots: one common pathway for all angiosperms? Int. J. Plant Dev. Biol. 1, 212–225 (2007).

    Google Scholar 

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Acknowledgements

We thank G. Den Herder, D. Van Damme and two anonymous referees for critical reading of the manuscript and useful suggestions, W. Grunewald, L. Smith, R. Quatrano, D. Twell, M. F. Njo, R. De Rycke and J. Dong for providing pictures and G. Van Isterdael for preparing the figures. We apologize to those colleagues whose work could not be included because of space restrictions. This work was supported by the Biotechnology and Biological Sciences Research Council, UK (BBSRC David Phillips Fellowship to I.D.S.); the Research Foundation — Flanders, Belgium (postdoctoral fellowship to I.D.S.); and grants from the Interuniversity Attraction Poles Programme (P6/33 and P5/13), initiated by the Belgian State Science Policy Office (BELSPO).

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Authors and Affiliations

  1. Plant and Crop Sciences Division, School of Biosciences, University of Nottingham, Loughborough, LE12 5RD, UK

    Ive De Smet

  2. Department of Plant Systems Biology, VIB, Technologiepark 927, Gent, 9052, Belgium

    Ive De Smet & Tom Beeckman

  3. Department of Plant Biotechnology and Genetics, Ghent University, Technologiepark 927, Gent, 9052, Belgium

    Ive De Smet & Tom Beeckman

  4. Tom Beeckman

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Glossary

Stem cell niche

The environment that provides signals and physical support to maintain stem cells.

Preprophase band

A modification of the plant cortical cytoskeleton in cells preparing to divide, consisting of a ring of actin and microtubules that transiently marks the plane of cell division.

Microspore

A developing pollen grain (male gametophyte) at the uninucleate stage within the microsporangia of the stamen in seed plants.

Thallic tissue

The body of an alga (thallus).

Rhizoid tissue

A branching, filamentous, root-like extension by which algae can attach to a substrate and absorb water and nutrients.

Suspensor

A terminally differentiated embryonic cell file that connects the embryo to surrounding tissues during early seed development.

Hypophysis

The uppermost cell of the basal lineage, called the suspensor, which will give rise to the root meristem.

Dermatogen stage

The embryonic stage during which tangential cell divisions occur, creating tissue layers following the octant stage.

Protoderm

The outer layer that will become the epidermis.

Stomata

A structure in the epidermis of aerial organs that balances gas exchange and water loss.

Anticlinal cell division

A division at a right angle to the surface of an organ or plant part.

Pericycle

The outermost tissue of the stele (that is, the central column of vascular and supporting tissues), which lies underneath the endodermis.

Procambium

A strand of meristematic stem cells that give rise to the vasculature.

Periclinal division

A type of cell division that occurs parallel to an adjacent layer of cells and/or to the surface of a plant part.

Symplastic movement

Movement through the continuous connection of cytoplasm through plasmodesmata.

Auxin response factor

A transcription factor that regulates auxin-responsive gene expression, the activity of which is repressed upon heterodimerization with AUXIN/INDOLE-3-ACETIC ACID repressor proteins.

Auxin

A plant hormone that regulates various aspects of plant growth and development.

Lateral root founder cell

A pericycle cell that initiates lateral root primordia.

Protoxylem

The first-formed xylem that develops from the procambium.

PAR–aPKC complex

(Partitioning defective–atypical protein kinase C complex). Part of an evolutionarily conserved molecular cassette, which has fundamental roles in cell polarity and many other biological contexts in animals.

Female gametophyte

A multicellular haploid structure that develops into an embryo and endosperm after fertilization.

Silica cell

A short cell that posseses a silica body (phytolith) in the epidermis of grasses.

Phragmoplast

A plant-specific cytoskeletal structure that consists of two sets of parallel microtubules and actin filaments, between which the cell plate forms by transport of cell-plate forming vesicles to the centre.

SCF

(SKP1–cullin–F-box). A ubiquitin protein ligase complex that functions in protein degradation.

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De Smet, I., Beeckman, T. Asymmetric cell division in land plants and algae: the driving force for differentiation. Nat Rev Mol Cell Biol 12, 177–188 (2011). https://doi.org/10.1038/nrm3064

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