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Plant trichomes: a model for cell differentiation

Nature Reviews Molecular Cell Biology volume 5, pages 471–480 (2004)Cite this article

Key Points

  • Analysis of the single-celled Arabidopsis thaliana trichomes has provided insights into several general cellular processes and machineries, including the function of transcription factors, cell-cycle regulation, the control of the microtubule and actin cytoskeleton, and cell-death control.

  • Trichome patterning begins with cells that are initially equivalent. A pattern is generated through cell–cell communication between neighbouring cells, which is mediated by the movement of small MYB-like proteins that interact with a complex that comprises a MYB-like transcription factor, a basic helix–loop–helix (HLH) protein and a WD40 protein.

  • Trichomes are polyploid, and overexpression studies and mutants enabled the analysis of how the switch from mitosis to endoreduplication is regulated and how the number of cycles is controlled.

  • Trichome branching is controlled by at least four different pathways, which involve microtubules, cell growth or one of two genes — ANGUSTIFOLIA (which is involved in transcriptional regulation or Golgi-dependent processes) or STICHEL (which has unknown biochemical properties).

  • The directionality of cell expansion is controlled by the actin-modulating ARP2/3 complex.

  • Analysis of these different processes in one model cell type offers the possibility to explore how seemingly unrelated processes might be interconnected during development.

Abstract

During the past few years, the focus in plant developmental biology has shifted from studying the organization of the whole body or individual organs towards the behaviour of the smallest unit of the organism, the single cell. Plant leaf hairs, or trichomes, serve as an excellent model system to study all aspects of plant differentiation at the single-cell level, including the choice of cell fate, developmental control of the cell cycle, cell polarity and the control of cell shape.

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Figure 1: Trichome development.
Figure 2: Redundancy of trichome-patterning genes.
Figure 3: Regulation of the cell cycle in trichomes.
Figure 4: Regulation of trichome branching.
Figure 5: Control of expansion polarity.

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References

  1. Esau, K. Anatomy of Seed Plants (John Wiley & Sons, New York, 1977).

    Google Scholar 

  2. Uphof, J. C. T. Plant hairs (eds. Zimmermann, W. & Ozenda, P. G.) (Gebr. Bornträger, Berlin, 1962).

    Google Scholar 

  3. Johnson, H. B. Plant pubescence: an ecological perspective. Bot. Rev. 41, 233–258 (1975).

    Article  Google Scholar 

  4. Mauricio, R. & Rausher, M. D. Experimental manipulation of putative selective agents provides evidence for the role of natural enemies in the evolution of plant defense. Evolution 51, 1435–1444 (1997).

    Article  PubMed  Google Scholar 

  5. Marks, M. D. Molecular genetic analysis of trichome development in Arabidopsis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48, 137–163 (1997).

    Article  CAS  PubMed  Google Scholar 

  6. Hülskamp, M., Schnittger, A. & Folkers, U. Pattern formation and cell differentiation: trichomes in Arabidopsis as a genetic model system. Int. Rev. Cytol. 186, 147–178 (1999).

    Article  PubMed  Google Scholar 

  7. Hülskamp, M., Misera, S. & Jürgens, G. Genetic dissection of trichome cell development in Arabidopsis. Cell 76, 555–566 (1994). Trichome development was dissected into discrete developmental steps using a systematic mutagenesis screen.

    Article  PubMed  Google Scholar 

  8. Larkin, J. C., Young, N., Prigge, M. & Marks, M. D. The control of trichome spacing and number in Arabidopsis. Development 122, 997–1005 (1996). Elegant demonstration that trichome spacing does not involve cell lineage.

    CAS  PubMed  Google Scholar 

  9. Melaragno, J. E., Mehrotra, B. & Coleman, A. W. Relationship between endopolyploidy and cell size in epidermal tissue of Arabidopsis. Plant Cell 5, 1661–1668 (1993).

    Article  PubMed  PubMed Central  Google Scholar 

  10. Folkers, U., Berger, J. & Hülskamp, M. Cell morphogenesis of trichomes in Arabidopsis: differential control of primary and secondary branching by branch initiation regulators and cell growth. Development 124, 3779–3786 (1997).

    CAS  PubMed  Google Scholar 

  11. Schnittger, A., Folkers, U., Schwab, B., Jürgens, G. & Hülskamp, M. Generation of a spacing pattern: the role of TRIPTYCHON in trichome patterning in Arabidopsis. Plant Cell 11, 1105–1116 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Hülskamp, M. & Schnittger, A. Spatial regulation of trichome formation in Arabidopsis thaliana. Semin. Cell Dev. Biol. 9, 213–220 (1998).

    Article  PubMed  Google Scholar 

  13. Scheres, B. Plant patterning: TRY to inhibit your neighbors. Curr. Biol. 12, R804–R806 (2002).

    Article  CAS  PubMed  Google Scholar 

  14. Schiefelbein, J. Cell-fate specification in the epidermis: a common patterning mechanism in the root and shoot. Curr. Opin. Plant Biol. 6, 74–78 (2003).

    Article  CAS  PubMed  Google Scholar 

  15. Larkin, J. C., Brown, M. L. & Schiefelbein, J. How do cells know what they want to be when they grow up? Lessons from epidermal patterning in Arabidopsis. Annu. Rev. Plant Biol. 54, 403–430 (2003).

    Article  CAS  PubMed  Google Scholar 

  16. Koornneef, M., Dellaert, L. W. M. & van der Veen, J. H. EMS- and radiation-induced mutation frequencies at individual loci in Arabidopsis thaliana. Mutat. Res. 93, 109–123 (1982).

    Article  CAS  PubMed  Google Scholar 

  17. Koornneef, M. The complex syndrome of ttg mutants. Arabidopsis Information Service 18, 45–51 (1981).

    Google Scholar 

  18. Zhang, F., Gonzalez, A., Zhao, M., Payne, C. T. & Lloyd, A. A network of redundant bHLH proteins functions in all TTG1-dependent pathways of Arabidopsis. Development 130, 4859–4869 (2003). Excellent analysis of how the many functions of TTG1 are mediated by a partially redundant network of bHLH and MYB transcription factors.

    Article  CAS  PubMed  Google Scholar 

  19. Schellmann, S. et al. TRIPTYCHON and CAPRICE mediate lateral inhibition during trichome and root hair patterning in Arabidopsis. EMBO J. 21, 5036–5046 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Wada, T., Tachibana, T., Shimura, Y. & Okada, K. Epidermal cell differentiation in Arabidopsis determined by a myb homolog, CPC. Science 277, 1113–1116 (1997).

    Article  CAS  PubMed  Google Scholar 

  21. Kirik, V., Simon, M., Hülskamp, M. & Schiefelbein, J. The ENHANCER OF TRY AND CPC1 (ETC1) gene acts redundantly with TRIPTYCHON and CAPRICE in trichome and root hair cell patterning in Arabidopsis. Dev. Biol. 268, 506–513 (2004).

    Article  CAS  PubMed  Google Scholar 

  22. Payne, C. T., Zhang, F. & Lloyd, A. M. GL3 encodes a bHLH protein that regulates trichome development in Arabidopsis through interaction with GL1 and TTG1. Genetics 156, 1349–1362 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Oppenheimer, D. G., Herman, P. L., Sivakumaran, S., Esch, J. & Marks, M. D. A myb gene required for leaf trichome differentiation in Arabidopsis is expressed in stipules. Cell 67, 483–493 (1991).

    Article  CAS  PubMed  Google Scholar 

  24. Walker, A. R. et al. The TRANSPARENT TESTA GLABRA1 locus, which regulates trichome differentiation and anthocyanin biosynthesis in Arabidopsis, encodes a WD40 repeat protein. Plant Cell 11, 1337–1349 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Szymanski, D. B., Lloyd, A. M. & Marks, M. D. Progress in the molecular genetic analysis of trichome intiation and morphogenesis in Arabidopsis. Trends Plant Sci. 5, 214–219 (2000).

    Article  CAS  PubMed  Google Scholar 

  26. Esch, J. J. et al. A contradictory GLABRA3 allele helps define gene interactions controlling trichome development in Arabidopsis. Development 130, 5885–5894 (2003). First insight into how the negative regulator TRY might counteract the GL1–GL3–TTG1 complex. Yeast three-hybrid analysis showed that TRY competes with GL1 for binding to GL3.

    Article  CAS  PubMed  Google Scholar 

  27. Wada, T. et al. Role of a positive regulator of root hair development, CAPRICE, in Arabidopsis root epidermal cell differentiation. Development 129, 5409–5419 (2002).

    Article  CAS  PubMed  Google Scholar 

  28. Lee, M. M. & Schiefelbein, J. Cell patterning in the Arabidopsis root epidermis determined by lateral inhibition with feedback. Plant Cell 14, 611–618 (2002). Elegant molecular-genetic study that is the first to show a regulatory feedback mechanism during root-hair patterning.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Rerie, W. G., Feldmann, K. A. & Marks, M. D. The glabra 2 gene encodes a homeo domain protein required for normal trichome development in Arabidopsis. Genes Dev. 8, 1388–1399 (1994).

    Article  CAS  PubMed  Google Scholar 

  30. Cristina, M. D. et al. The Arabidopsis Athb-10 (GLABRA2) is an HD-Zip protein required for regulation of root hair development. Plant J. 10, 393–402 (1996).

    Article  CAS  PubMed  Google Scholar 

  31. Szymanski, D. B., Jilk, R. A., Pollock, S. M. & Marks, M. D. Control of GL2 expression in Arabidopsis leaves and trichomes. Development 125, 1161–1171 (1998).

    CAS  PubMed  Google Scholar 

  32. Ohashi, Y., Oka, A., Ruberti, I., Morelli, G. & Aoyama, T. Entopically additive expression of GLABRA2 alters the frequency and spacing of trichome initiation. Plant J. 29, 359–369 (2002).

    Article  CAS  PubMed  Google Scholar 

  33. Ohashi, Y. et al. Modulation of phospholipid signaling by GLABRA2 in root-hair pattern formation. Science 300, 1427–1430 (2003). Identification of the first gene that functions downstream of the patterning machinery.

    Article  CAS  PubMed  Google Scholar 

  34. Walker, J. D., Oppenheimer, D. G., Concienne, J. & Larkin, J. C. SIAMESE, a gene controlling the endoreduplication cell cycle in Arabidopsis thaliana trichomes. Development 127, 3931–3940 (2000).

    CAS  PubMed  Google Scholar 

  35. Schnittger, A., Schobinger, U., Stierhof, Y. D. & Hülskamp, M. Ectopic B-type cyclin expression induces mitotic cycles in endoreduplicating Arabidopsis trichomes. Curr. Biol. 12, 415–420 (2002).

    Article  CAS  PubMed  Google Scholar 

  36. Schnittger, A. et al. Ectopic D-type cyclin expression induced not only DNA replication but also cell division in Arabidopsis trichomes. Proc. Natl Acad. Sci. USA 99, 6410–5415 (2002). Overexpression studies showed that plant D-type cyclins function, not only at the G1 transition, but also at the entry of mitosis.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Sugimoto-Shirasu, K., Stacey, N. J., Corsar, J., Roberts, K. & McCann, M. C. DNA topoisomerase VI is essential for endoreduplication in Arabidopsis. Curr. Biol. 12, 1782–1786 (2002).

    Article  CAS  PubMed  Google Scholar 

  38. Jacobsen, S. E., Binkowski, K. A. & Olszewski, N. E. SPINDLY, a tetratricopeptide repeat protein involved in gibberellin signal transduction in Arabidopsis. Proc. Natl Acad. Sci. USA 93, 9292–9296 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Chien, J. C. & Sussex, I. M. Differential regulation of trichome formation on the adaxial and abaxial leaf surfaces by gibberellins and photoperiod in Arabidopsis thaliana (L.) Heynh. Plant Physiol. 111, 1321–1328 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Telfer, A., Bollman, K. M. & Poethig, R. S. Phase change and the regulation of trichome distribution in Arabidopsis thaliana. Development 124, 645–654 (1997).

    CAS  PubMed  Google Scholar 

  41. Downes, B. P., Stupar, R. M., Gingerich, D. J. & Vierstra, R. D. The HECT ubiquitin-protein ligase (UPL) family in Arabidopsis: UPL3 has a specific role in trichome development. Plant J. 35, 729–742 (2003).

    Article  CAS  PubMed  Google Scholar 

  42. El Refy, A. et al. The Arabidopsis KAKTUS gene encodes a HECT protein and controls the number of endoreduplication cycles. Mol. Genet. Genomics 270, 403–414 (2004).

    Article  CAS  Google Scholar 

  43. Hülskamp, M. How plants split hairs. Curr. Biol. 10, R308–R310 (2000).

    Article  PubMed  Google Scholar 

  44. Krishnakumar, S. & Oppenheimer, D. G. Extragenic suppressors of the Arabidopsis zwi-3 mutation identify new genes that function in trichome branch formation and pollen tube growth. Development 126, 3079–3088 (1999).

    CAS  PubMed  Google Scholar 

  45. Oppenheimer, D. Genetics of plant cell shape. Curr. Opin. Plant Biol. 1, 520–524 (1998).

    Article  CAS  PubMed  Google Scholar 

  46. Luo, D. & Oppenheimer, D. G. Genetic control of trichome branch number in Arabidopsis: the roles of the FURCA loci. Development 126, 5547–5557 (1999). Detailed genetic studies on the genetic interactions between the branching genes showed that they function largely in independent pathways.

    CAS  PubMed  Google Scholar 

  47. Perazza, D. et al. Trichome cell growth in Arabidopsis thaliana can be depressed by mutations in at least five genes. Genetics 152, 461–476 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Kirik, V. et al. CPR5 is involved in cell proliferation and cell death control and encodes a novel transmembrane protein. Curr. Biol. 11, 1891–1895 (2001).

    Article  CAS  PubMed  Google Scholar 

  49. Mathur, J. & Chua, N. -H. Microtubule stabilization leads to growth reorientation in Arabidopsis thaliana trichomes. Plant Cell 12, 465–477 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Kirik, V. et al. The Arabidopsis TUBULIN-FOLDING COFACTOR A gene is involved in the control of the α/β-tubulin monomer balance. Plant Cell 14, 2265–2276 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Kirik, V. et al. Functional analysis of the tubulin-folding cofactor C in Arabidopsis thaliana. Curr. Biol. 12, 1519–1523 (2002).

    Article  CAS  PubMed  Google Scholar 

  52. Steinborn, K. et al. The Arabidopsis PILZ group genes encode tubulin-folding cofactor orthologs required for cell division but not cell growth. Genes Dev. 16, 959–971 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Bichet, A., Desnos, T., Turner, S., Grandjean, O. & Höfte, H. BOTERO1 is required for normal orientation of cortical microtubules and anisotropic cell expansion in Arabidopsis. Plant J. 25, 137–148 (2001).

    Article  CAS  PubMed  Google Scholar 

  54. Webb, M., Jouannic, S., Foreman, J., Linstead, P. & Dolan, L. Cell specification in the Arabidopsis root epidermis requires the activity of ECTOPIC ROOT HAIR 3 — a katanin-p60 protein. Development 129, 123–131 (2002).

    CAS  PubMed  Google Scholar 

  55. Burk, D. H., Liu, B., Zhong, R., Morrison, W. H. & Ye, Z. H. A katanin-like protein regulates normal cell wall biosynthesis and cell elongation. Plant Cell 13, 807–827 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  57. Traas, J. et al. Normal differentiation patterns in plants lacking microtubular preprophase bands. Nature 375, 676–677 (1995).

    Article  CAS  Google Scholar 

  58. Camilleri, C. et al. The Arabidopsis TONNEAU2 gene encodes a putative novel protein phosphatase 2A regulatory subunit essential for the control of the cortical cytoskeleton. Plant Cell 14, 833–845 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Qiu, J. L., Jilk, R., Marks, M. D. & Szymanski, D. B. The Arabidopsis SPIKE1 gene is required for normal cell shape control and tissue development. Plant Cell 14, 101–118 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Brugnera, E. et al. Unconventional Rac-GEF activity is mediated through the Dock180–ELMO complex. Nature Cell Biol. 4, 574–582 (2002).

    Article  CAS  PubMed  Google Scholar 

  61. Deeks, M. J. & Hussey, P. J. Arp2/3 and 'the shape of things to come'. Curr. Opin. Plant Biol. 6, 561–567 (2003). Excellent review on the possible role and regulation of actin through the ARP2/3 complex.

    Article  CAS  PubMed  Google Scholar 

  62. Reddy, A. S., Narasimhulu, S. B., Safadi, F. & Golovkin, M. A plant kinesin heavy chain-like protein is a calmodulin-binding protein. Plant J. 10, 9–21 (1996).

    Article  CAS  PubMed  Google Scholar 

  63. Reddy, A. S. N., Safadi, F., Narasimhulu, S. B., Golovkin, M. & Hu, X. A novel plant calmodulin-binding protein with a kinesin heavy chain motor domain. J. Biol. Chem. 271, 7052–7060 (1996).

    Article  CAS  PubMed  Google Scholar 

  64. Reddy, A. S. N., Narasimhulu, S. B. & Day, I. S. Structural organization of a gene encoding a novel calmodulin-binding kinesin-like protein from Arabidopsis. Gene 204, 195–200 (1997).

    Article  CAS  PubMed  Google Scholar 

  65. Song, H., Golovkin, M., Reddy, A. S. & Endow, S. A. In vitro motility of AtKCBP, a calmodulin-binding kinesin protein of Arabidopsis. Proc. Natl Acad. Sci. USA 94, 322–237 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Deavours, B. E., Reddy, A. S. & Walker, R. A. Ca2+/calmodulin regulation of the Arabidopsis kinesin-like calmodulin-binding protein. Cell Motil. Cytoskeleton 40, 408–416 (1998).

    Article  CAS  PubMed  Google Scholar 

  67. Oppenheimer, D. G. et al. Essential role of a kinesin-like protein in Arabidopsis trichome morphogenesis. Proc. Natl Acad. Sci. USA 94, 6261–6266 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Reddy, V. S., Day, I., Thomas, T. & Reddy, A. S. N. KIC, a novel Ca2+ binding protein with one EF-hand motif, interacts with a microtubule motor protein and regulates trichome morphogenesis. Plant Cell 16, 185–200 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Folkers, U. et al. The cell morphogenesis gene ANGUSTIFOLIA encodes a CtBP/BARS-like protein and is involved in the control of the microtubule cytoskeleton. EMBO J. 21, 1280–1288 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Kim, G. T. et al. The ANGUSTIFOLIA gene of Arabidopsis, a plant CtBP gene, regulates leaf-cell expansion, the arrangement of cortical microtubules in leaf cells and expression of a gene involved in cell-wall formation. EMBO J. 26, 1267–1279 (2002).

    Article  Google Scholar 

  71. Nibu, Y., Zhang, H. & Levine, M. Interaction of a short-range repressors with Drosophila CtBP in the embryo. Science 280, 101–104 (1998).

    Article  CAS  PubMed  Google Scholar 

  72. Matteis, M. D. et al. Stimulation of endogenous ADP-ribosylation by brefeldin A. Proc. Natl Acad. Sci. USA 91, 1114–1118 (1994).

    Article  PubMed  PubMed Central  Google Scholar 

  73. Lippincott-Schwartz, J., Yuan, L. C., Bonifacino, J. S. & Klausner, R. D. Rapid redistribution of Golgi proteins into the ER in cells treated with brefeldin A: evidence for membrane cycling from Golgi to ER. Cell 56, 801–813 (1989).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Ilgenfritz, H. et al. The Arabidopsis STICHEL gene is a regulator of trichome branch number and encodes a novel protein. Plant Physiol. 131, 643–655 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Szymanski, D. B., Marks, M. D. & Wick, S. M. Organized F-actin is essential for normal trichome morphogenesis in Arabidopsis. Plant Cell 11, 2331–2348 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Schwab, B. et al. Regulation of cell expansion by the DISTORTED genes in Arabidopsis thaliana: actin controls the spatial organization of microtubules. Mol. Genet. Genomics 269, 350–360 (2003).

    Article  CAS  PubMed  Google Scholar 

  77. Mathur, J., Spielhofer, P., Kost, B. & Chua, N. -H. The actin cytoskeleton is required to elaborate and maintain spatial patterning during trichome cell morphogenesis in Arabidopsis thaliana. Development 126, 5559–5568 (1999).

    CAS  PubMed  Google Scholar 

  78. Mathur, J. et al. Arabidopsis CROOKED encodes for the smallest subunit of the ARP2/3 complex and controls cell shape by region specific fine F-actin formation. Development 130, 3137–3146 (2003).

    Article  CAS  PubMed  Google Scholar 

  79. Mathur, J., Mathur, N., Kernebeck, B. & Hülskamp, M. Mutations in actin-related proteins 2 and 3 affect cell shape development in Arabidopsis. Plant Cell 15, 1632–1645 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Le, J., El-Assal Sel, D., Basu, D., Saad, M. E. & Szymanski, D. B. Requirements for Arabidopsis ATARP2 and ATARP3 during epidermal development. Curr. Biol. 13, 1341–1347 (2003).

    Article  CAS  PubMed  Google Scholar 

  81. Li, S., Blanchoin, L., Yang, Z. & Lord, E. M. The putative Arabidopsis arp2/3 complex controls leaf cell morphogenesis. Plant Physiol. 132, 2034–2044 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Mullins, R. D., Heuser, J. A. & Pollard, T. D. The interaction of Arp2/3 complex with actin: nucleation, high affinity pointed end capping, and formation of branching networks of filaments. Proc. Natl Acad. Sci. USA 95, 6181–6186 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Svitkina, T. M. & Borisy, G. G. ARP2/3 complex and actin depolymerizing factor/cofilin in dendritic organization and treadmilling of actin filament array in lamellipodia. J. Cell Biol. 145, 1009–1026 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Mathur, J. & Hülskamp, M. Signal transduction: Rho-like proteins in plants. Curr. Biol. 12, R526–R528 (2002).

    Article  CAS  PubMed  Google Scholar 

  85. Smith, L. G. Cytoskeletal control of plant cell shape: getting the fine points. Curr. Opin. Plant Biol. 6, 63–73 (2003).

    Article  PubMed  Google Scholar 

  86. Yang, Z. Small GTPases: versatile signaling switches in plants. Plant Cell 14 (Suppl.) 375–388 (2002).

    Article  CAS  Google Scholar 

  87. De Veylder, L. et al. Functional analysis of cyclin-dependent kinase inhibitors of Arabidopsis. Plant Cell 13, 1653–1668 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Hiromura, K., Pippin, J. W., Fero, M. L., Roberts, J. M. & Shankland, S. J. Modulation of apoptosis by the cyclin-dependent kinase inhibitor p27(Kip1). J. Clin. Invest. 103, 597–604 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Wang, H. et al. ICK1, a cyclin-dependent protein kinase inhibitor from Arabidopsis thaliana interacts with both Cdc2a and CycD3, and its expression is induced by abscisic acid. Plant J. 15, 501–510 (1998).

    Article  PubMed  Google Scholar 

  90. Jasinski, S. et al. The CDK inhibitor NtKIS1a is involved in plant development, endoreduplication and restores normal development of cyclin D3;1-overexpressing plants. J. Cell Sci. 115, 973–982 (2002).

    CAS  PubMed  Google Scholar 

  91. Schnittger, A., Weinl, C., Bouyer, D., Schobinger, U. & Hülskamp, M. Misexpression of the cyclin-dependent kinase inhibitor ICK1/KRP1 in single-celled Arabidopsis trichomes reduces endoreduplication and cell size and induces cell death. Plant Cell 15, 303–315 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Glazebrook, J. Genes controlling expression of defense responses in Arabidopsis — 2001 status. Curr. Opin. Plant Biol. 4, 301–308 (2001).

    Article  CAS  PubMed  Google Scholar 

  93. Haughn, G. W. & Somerville, C. R. Genetic control of morphogenesis in Arabidopsis. Dev. Genet. 9, 73–89 (1988).

    Article  Google Scholar 

  94. Potikha, T. & Delmer, D. A mutant of Arabidopsis thaliana displaying altered patterns of cellulose deposition. Plant J. 7, 453–460 (1995).

    Article  CAS  Google Scholar 

  95. Meinhardt, H. & Gierer, A. Applications of a theory of biological pattern formation based on lateral inhibition. J. Cell Sci. 15, 321–346 (1974).

    CAS  PubMed  Google Scholar 

  96. Vos, J. W., Safadi, F., Reddy, A. S. & Hepler, P. K. The kinesin-like calmodulin binding protein is differentially involved in cell division. Plant Cell 12, 979–990 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Bowser, J. & Reddy, A. S. N. Localization of a kinesin-like calmodulin-binding protein in dividing cells of Arabidopsis and tobacco. Plant J. 12, 1429–1437 (1997).

    Article  CAS  PubMed  Google Scholar 

  98. Schwab, B., Folkers, U., Ilgenfritz, H., and Hülskamp, M. Trichome morphogenesis in Arabidopsis. Philos. Trans. R. Soc. Lond. B 355, 879–883 (2000).

    Article  CAS  Google Scholar 

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Acknowledgements

I would like to thank H. Meinhardt for providing the images and the movie that are presented in Box 1 and for stimulating discussions. I would also like to thank the members of the laboratory for helpful comments on the manuscript. Research in the author's laboratory is supported by the Deutsche Forschungsgemeinschaft and the Volkswagen Stiftung.

Author information

Authors and Affiliations

  1. University of Köln, Botanical Institute III, Gyrhofstraße 15, Köln, 50931, Germany

    Martin Hülskamp

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  1. Martin Hülskamp
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Supplementary information

41580_2004_BFnrm1404_MOESM1_ESM.gif

supplementary information S1S1 (movie) | The Gierer-Meinhardt model. The movie illustrates how a de novo pattern is generated according to this theoretical model. The top panel shows the spatial distribution of the activity of the activator and the bottom panel shows that of the inhibitor. Please note that maximum activities of the activator and the inhibitor colocalize. This movie is courtesy of H. Meinhardt. (GIF 399 kb)

41580_2004_BFnrm1404_MOESM2_ESM.mp4

supplementary information S2S2 (movie) | Peroxisome movement in a wild-type trichome. A wild-type trichome that expresses peroxisome-targeted green fluorescent protein (GFP) is shown. Peroxisome movement depends on the actin cytoskeleton and in the wild-type trichome, peroxisomes move rapidly over long distances. This movie is courtesy of J. Mathur. (MP4 123 kb)

41580_2004_BFnrm1404_MOESM3_ESM.mov

supplementary information S3S3 (movie) | Peroxisome movement in a crooked-mutant trichome. A crooked-mutant trichome that expresses peroxisometargeted green fluorescent protein (GFP) is shown. Peroxisome movement depends on the actin cytoskeleton and the movie shows that, despite the defects in the actin organization, peroxisome movement is not generally affected. This movie is courtesy of J. Mathur. (MOV 2056 kb)

Related links

Related links

DATABASES

TAIR

AN

CPC

CPR5

CYCB1;2

CYCD3;1

EGL3

GL1

GL2

GL3

HYP6

KAK

RHL2

SIM

STI

TTG1

WER

ZWI

Glossary

ENDOREDUPLICATION

A modified cell cycle in which DNA replication continues in the absence of mitosis and cytokinesis.

PROTODERMAL CELL

A young epidermal cell that has not yet differentiated into a specialized cell type.

MYB-RELATED TRANSCRIPTION FACTOR

A transcription factor that contains a DNA-binding domain that shows sequence similarity to vMYB, the first-described member of this family.

BASIC HELIX–LOOP–HELIX (BHLH) FACTOR

A protein that contains two α-helices separated by a loop (the HLH domain), which binds DNA in a sequence-specific manner.

WD40 PROTEIN

A 40-amino-acid-long protein motif that contains a WD dipeptide at its carboxy terminus. This domain is found in many functionally diverse proteins and mediates protein–protein interactions.

CORTEX CELL

The tissue between the vascular bundle and the epidermis. In A. thaliana, this is a single cell layer.

PLASMODESMATA

Cell–cell connections in plants through which macromolecules, including RNA and proteins, can be transported in a regulated manner.

B-TYPE AND D-TYPE CYCLINS

Cyclins regulate cell-cycle progression through interactions with cyclin-dependent protein kinases. B-type cyclins regulate entry into mitosis, whereas D-type cyclins are important in G1 phase and, in plants, also for entry into mitosis.

DNA TOPOISOMERASE

An enzyme that can cleave and religate the DNA to allow a more relaxed DNA configuration.

DECATENATE

During DNA replication, sister duplex molecules become interlinked (catenated). Decatenation is the separation of two entangled chromosomes.

UBIQUITIN E3 LIGASE

An enzyme that attaches ubiquitin to a protein, thereby marking it for degradation in the proteasome.

PRE-PROPHASE BAND

A dense band of microtubules at the cell cortex that appears before the start of cell division in plants. Its position marks the future division plane.

PHRAGMOPLAST

A fibrous structure between the daughter nuclei at telophase in plant cells; also known as the cell plate.

ARP2/3 COMPLEX

(Actin-related protein 2/3). A multi-protein complex that consists of seven different proteins and initiates new actin filaments on pre-existing ones.

CHROMOCENTRE

A region in plant chromosomes that comprises heterochromatin and coincides with centromeres during meiosis.

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Hülskamp, M. Plant trichomes: a model for cell differentiation. Nat Rev Mol Cell Biol 5, 471–480 (2004). https://doi.org/10.1038/nrm1404

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