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Plant Cell Reports

, Volume 28, Issue 8, pp 1147–1157 | Cite as

Molecular mechanisms controlling pavement cell shape in Arabidopsis leaves

  • Pingping Qian
  • Suiwen Hou
  • Guangqin Guo
Review

Abstract

Pavement cells have an interlocking jigsaw puzzle-shaped leaf surface pattern. Twenty-three genes involved in the pavement cell morphogenesis were discovered until now. The mutations of these genes through various means lead to pavement cell shape defects, such as loss or lack of interdigitation, the reduction of lobing, gaps between lobe and neck regions in pavement cells, and distorted trichomes. These phenotypes are affected by the organization of microtubules and microfilaments. Microtubule bands are considered corresponding with the neck regions of the cell, while lobe formation depends on patches of microfilaments. The pathway of Rho of plant (ROP) GTPase signaling cascades regulates overall activity of the cytoskeleton in pavement cells. Some other proteins, in addition to the ROPs, SCAR/WAVE, and ARP2/3 complexes, are also involved in the pavement cell morphogenesis.

Keywords

Arabidopsis Morphogenesis Pavement cell Cytoskeleton ARP2/3 SCAR/WAVE ROP 

Notes

Acknowledgments

This work is supported by the National Basic Research Program of China (grant no. 2009CB941500), the National Natural Science Foundation of China (NSFC) (grant no. 30670124), and program for New Century Excellent Talents of the Ministry of Education (grant no. NCET-06-0897).

References

  1. Basu D, El-Assal Sel D, Le J, Mallery EL, Szymanski DB (2004) Interchangeable functions of Arabidopsis PIROGI and the human WAVE complex subunit SRA1 during leaf epidermal development. Development 131:4345–4355PubMedCrossRefGoogle Scholar
  2. Basu D, Le J, El-Essal Sel D, Huang S, Zhang C, Mallery EL, Koliantz G, Staiger CJ, Szymanski DB (2005) DISTORTED3/SCAR2 is a putative arabidopsis WAVE complex subunit that activates the Arp2/3 complex and is required for epidermal morphogenesis. Plant Cell 17:502–524PubMedCrossRefGoogle Scholar
  3. Basu D, Le J, Zakharova T, Mallery EL, Szymanski DB (2008) A SPIKE1 signaling complex controls actin-dependent cell morphogenesis through the heteromeric WAVE and ARP2/3 complexes. Proc Natl Acad Sci USA 105:4044–4049PubMedCrossRefGoogle Scholar
  4. Bichet A, Desnos T, Turner S, Grandjean O, Hofte H (2001) BOTERO1 is required for normal orientation of cortical microtubules and anisotropic cell expansion in Arabidopsis. Plant J 25:137–148PubMedCrossRefGoogle Scholar
  5. Blanchoin L, Amann KJ, Higgs HN, Marchand JB, Kaiser DA, Pollard TD (2000) Direct observation of dendritic actin filament networks nucleated by Arp2/3 complex and WASP/Scar proteins. Nature 404:1007–1011PubMedCrossRefGoogle Scholar
  6. Bouquin T, Mattsson O, Naested H, Foster R, Mundy J (2003) The Arabidopsis lue1 mutant defines a katanin p60 ortholog involved in hormonal control of microtubule orientation during cell growth. J Cell Sci 116:791–801PubMedCrossRefGoogle Scholar
  7. Bouton S, Leboeuf E, Leydecker MT, Talbotec J, Granier F, Lahaye M, Hofte H, Truong HN (2002) QUASIMODO1 encodes a putative membrane-bound glycosyltransferase required for normal pectin synthesis and cell adhesion in Arabidopsis. Plant Cell 14:2577–2590PubMedCrossRefGoogle Scholar
  8. Burk DH, Liu B, Zhong R, Morrison WH, Ye ZH (2001) A katanin-like protein regulates normal cell wall biosynthesis and cell elongation. Plant Cell 13:807–827PubMedCrossRefGoogle Scholar
  9. Carol RJ, Takeda S, Linstead P, Durrant MC, Kakesova H, Derbyshire P, Drea S, Zarsky V, Dolan L (2005) A RhoGDP dissociation inhibitor spatially regulates growth in root hair cells. Nature 438:1013–1016PubMedCrossRefGoogle Scholar
  10. Chary SN, Hicks GR, Choi YG, Carter D, Raikhel NV (2008) Trehalose-6-phosphate synthase/phosphatase regulates cell shape and plant architecture in Arabidopsis. Plant Physiol 146:97–107PubMedCrossRefGoogle Scholar
  11. Chisholm AD, Hardin J (2005) Epidermal morphogenesis. In: WormBook. The C. elegans Research CommunityGoogle Scholar
  12. Cooper JA, Wear MA, Weaver AM (2001) Arp2/3 complex: advances on the inner workings of a molecular machine. Cell 107:703–705PubMedCrossRefGoogle Scholar
  13. Deeks MJ, Hussey PJ (2003) ARP2/3 and ‘The shape of things to come’. Curr Opin Plant Biol 6:257–269CrossRefGoogle Scholar
  14. Deeks MJ, Kaloriti D, Davies B, Malho R, Hussey PJ (2004) Arabidopsis NAP1 is essential for Arp2/3-dependent trichome morphogenesis. Curr Biol 14:1410–1414PubMedCrossRefGoogle Scholar
  15. Djakovic S, Dyachok J, Burke M, Frank MJ, Smith LG (2006) BRICK1/HSPC300 functions with SCAR and the ARP2/3 complex to regulate epidermal cell shape in Arabidopsis. Development 133:1091–1100PubMedCrossRefGoogle Scholar
  16. Ebert B, Melle C, Lieckfeldt E, Zoller D, Eggeling F, Fisahn J (2008) Protein profiling of single epidermal cell types from Arabidopsis thaliana using surface-enhanced laser desorption and ionization technology. J Plant Physiol 165:1227–1237PubMedCrossRefGoogle Scholar
  17. El-Assal Sel D, Le J, Basu D, Mallery EL, Szymanski DB (2004a) Arabidopsis GNARLED encodes a NAP125 homolog that positively regulates ARP2/3. Curr Biol 14:1405–1409CrossRefGoogle Scholar
  18. El-Assal Sel D, Le J, Basu D, Mallery EL, Szymanski DB (2004b) DISTORTED2 encodes an ARPC2 subunit of the putative Arabidopsis ARP2/3 complex. Plant J 38:526–538CrossRefGoogle Scholar
  19. Falbel TG, Koch LM, Nadeau JA, Segui-Simarro JM, Sack FD, Bednarek SY (2003) SCD1 is required for cytokinesis and polarized cell expansion in Arabidopsis thaliana. Development 130:4011–4024PubMedCrossRefGoogle Scholar
  20. Folker U, Kirik V, Schobinger U, Falk S, Krishnakumar S, Pollock MA, Oppenheimer DG, Day I, Reddy AR (2002) The cell morphogenesis gene ANGUSTIFOLIA encodes a CtBP/BARS-like protein and is involved in the control of the microtubule cytoskeleton. EMBO J 21:1280–1288CrossRefGoogle Scholar
  21. Frank MJ, Smith LG (2002) A small, novel protein highly conserved in plants and animals promotes the polarized growth and division of maize leaf epidermal cells. Curr Biol 12:849–853PubMedCrossRefGoogle Scholar
  22. Frank M, Egile C, Dyachok J, Djakovic S, Nolasco M, Li R, Smith LG (2004) Activation of ARP2/3 complex-dependent actin polymerization by plant proteins distantly related to SCAR/WAVE. Proc Natl Acad Sci USA 101:16379–16384PubMedCrossRefGoogle Scholar
  23. Fu Y, Li H, Yang Z (2002) The ROP2 GTPase controls the formation of cortical fine F-actin and the early phase of directional cell expansion during Arabidopsis organogenesis. Plant Cell 14:777–794PubMedCrossRefGoogle Scholar
  24. Fu Y, Gu Y, Zheng Z, Wasteneys G, Yang Z (2005) Arabidopsis interdigitating cell growth requires two antagonistic pathways with opposing action on cell morphogenesis. Cell 120:687–700PubMedCrossRefGoogle Scholar
  25. Geisler M, Nadeau J, Sack FD (2000) Oriented asymmetric divisions that generate the stomatal spacing pattern in Arabidopsis are disrupted by the too many mouths mutation. Plant Cell 12:2075–2086PubMedCrossRefGoogle Scholar
  26. Guimil S, Dunand C (2007) Cell growth and differentiation in Arabidopsis epidermal cell. J Exp Bot 14:3829–3840CrossRefGoogle Scholar
  27. Higgs HN, Pollard TD (2001) Regulation of actin filament network formation through ARP2/3 complex: activation by a diverse array of proteins. Annu Rev Biochem 70:649–676PubMedCrossRefGoogle Scholar
  28. Horanic GE, Gardner FE (1967) An improved method of making epidermal imprints. Bot Gaz 128:144–150CrossRefGoogle Scholar
  29. Hulskamp M, Misera S, Jurgens G (1994) Genetic dissection of trichome cell development in Arabidopsis. Cell 76:555–566PubMedCrossRefGoogle Scholar
  30. Jaffe AB, Hall A (2005) Rho GTPases: biochemistry and biology. Annu Rev Cell Dev Biol 21:247–269PubMedCrossRefGoogle Scholar
  31. Kim GT, Shoda K, Tsuge T, Cho KH, Uchimiya H, Yokoyama R, Nishitani K, Tsukaya H (2002) 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 21:1267–1279PubMedCrossRefGoogle Scholar
  32. Kirik V, Bouyer D, Schobinger U, Bechtold N, Herzog M, Bonneville JM, Hulskamp M (2001) CPR5 is involved in cell proliferation and cell death control and encodes a novel transmembrane protein. Curr Biol 11:1891–1895PubMedCrossRefGoogle Scholar
  33. Kotzer AM, Wasteneys GO (2006) Mechanisms behind the puzzle: microtubule–microfilament cross-talk in pavement cell formation. Can J Bot 84:594–603CrossRefGoogle Scholar
  34. Lavy M, Bloch D, Hazak O, Gutman I, Poraty L, Sorek N, Sternberg H, Yalovsky S (2007) A novel ROP/RAC effector links cell polarity, root-meristem maintenance, and vesicle trafficking. Curr Biol 17:947–952PubMedCrossRefGoogle Scholar
  35. Le J, El-Assal SE, Basu D, Saad ME, Szymanksi DB (2003) Requirements for Arabidopsis ATARP2 and ATARP3 during epidermal development. Curr Biol 13:1341–1347PubMedCrossRefGoogle Scholar
  36. Lew DJ (2003) The morphogenesis checkpoint: how yeast cells watch their figures. Curr Opin Cell Biol 15:648–653PubMedCrossRefGoogle Scholar
  37. Li H, Shen J, Zheng Z, Lin Y, Yang Z (2001) The Rop GTPase switch controls multiple developmental processes in Arabidopsis. Plant Physiol 126:670–684PubMedCrossRefGoogle Scholar
  38. Li S, Blanchoin L, Yang Z, Lord EM (2003) The putative Arabidopsis arp2/3 complex controls leaf cell morphogenesis. Plant Physiol 132:2034–2044PubMedCrossRefGoogle Scholar
  39. Li Y, Sorefan K, Hemmann G, Bevan MW (2004) Arabidopsis NAP and PIR regulate actin-based cell morphogenesis and multiple developmental processes. Plant Physiol 136:3616–3627PubMedCrossRefGoogle Scholar
  40. Mathur J (2006) Local interactions shape plant cell. Curr Opin Cell Biol 18:40–46PubMedCrossRefGoogle Scholar
  41. Mathur J, Koncz C (1997) Method for preparation of epidermal imprints using agarose. Biotechnology 22:280–282Google Scholar
  42. Mathur J, Spielhofer P, Kost B, Chua N-H (1999) The actin cytoskeleton is required to elaborate and maintain spatial patterning during trichome cell morphogenesis in Arabidopsis thaliana. Development 126:5559–5568PubMedGoogle Scholar
  43. Mathur J, Mathur N, Kernebeck B, Hulskamp M (2003a) Mutations in actin-related proteins 2 and 3 affect cell shape development in Arabidopsis. Plant Cell 15:1632–1645PubMedCrossRefGoogle Scholar
  44. Mathur J, Mathur N, Kirik V, Kernebeck B, Srinivas BP, Hulskamp M (2003b) Arabidopsis CROOKED encodes for the smallest subunit of the ARP2/3 complex and controls cell shape by region specific fine F-actin formation. Development 130:3137–3146PubMedCrossRefGoogle Scholar
  45. McClinton RS, Chandler JS, Callis J (2001) cDNA isolation, characterization, and protein intracellular localization of a katanin-like p60 subunit from Arabidopsis thaliana. Protoplasma 216:181–190PubMedCrossRefGoogle Scholar
  46. Mullins RD, Heuser JA, Pollard TD (1998) 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 95:6181–6186PubMedCrossRefGoogle Scholar
  47. Panteris E, Galstis B (2005) The morphogenesis of lobed plant cells in the mesophyll and epidermis: organization and distinct roles of cortical microtubules and actin filament. New Phytol 167:721–732PubMedCrossRefGoogle Scholar
  48. Panteris E, Apostolakos P, Galatis B (1993) Microtubles and morphogenesis in ordinary epidermal cell of Vigna sinensis leaves. Protoplasma 174:91–100CrossRefGoogle Scholar
  49. Panteris E, Apostolakos P, Galatis B (1994) Sinuous ordinary epidermal cells—behind several patterns of waviness, a common morphogenetic mechanism. Protoplasma 127:771–780Google Scholar
  50. Parker JS, Cavell AC, Dolan L, Roberts K, Grierson CS (2000) Genetic interactions during root hair morphogenesis in Arabidopsis. Plant Cell 12:1961–1974PubMedCrossRefGoogle Scholar
  51. Qiu JL, Jilk R, Marks MD, Szymanski DB (2002) The Arabidopsis SPIKE1 gene is required for normal cell shape control and tissue development. Plant Cell 14:101–118PubMedCrossRefGoogle Scholar
  52. Ringli C, Bigler L, Kuhn BM, Leiber RM, Diet A, Santelia D, Frey B, Pollmann S, Klein M (2008) The modified flavonol glycosylation profile in the Arabidopsis rol1 mutants results in alterations in plant growth and cell shape formation. Plant Cell 20:1470–1481PubMedCrossRefGoogle Scholar
  53. Robinson RC, Turbedsky K, Kaiser DA, Marchand JB, Higgs HN, Choe S, Pollard TD (2001) Crystal structure of Arp2/3 complex. Science 294:1679–1684PubMedCrossRefGoogle Scholar
  54. Sampson J (1961) A method of replicating dry or moist surfaces for examination by light microscopy. Nature 191:932–933PubMedCrossRefGoogle Scholar
  55. Schwab B, Mathur J, Saedler R, Schwarz H, Frey B, Scheidegger C, Hulskamp M (2003) Regulation of cell expansion by the DISTORTED genes in Arabidopsis thaliana: actin controls the spatial organization of microtubules. Mol Genet Genom 269:350–360CrossRefGoogle Scholar
  56. Smith LG, Oppenheimer DG (2005) Spatial control of cell expansion by the plant cytoskeleton. Annu Rev Cell Dev Biol 21:271–295PubMedCrossRefGoogle Scholar
  57. Svitkina TM, Borisy GG (1999) Arp2/3 complex and actin depolymerizing factor/cofilin in dendritic organization and treadmilling of actin filament array in lamellipodia. J Cell Biol 145:1009–1026PubMedCrossRefGoogle Scholar
  58. Traas J, Hulskamp M, Gendreau E, Hofte H (1998) Endoreduplication and development: rule without dividing? Curr Opin Plant Biol 1:498–530PubMedCrossRefGoogle Scholar
  59. Uhrig JF, Mutondo M, Zimmermann I, Deeks MJ, Machesky LM, Thomas P, Uhrig S, Rambke C, Hussey PJ, Hulskamp M (2007) The role of Arabidopsis SCAR genes in ARP2-ARP3-dependent cell morphogenesis. Development 134:967–977PubMedCrossRefGoogle Scholar
  60. Wang X, Zhu L, Liu B, Wang C, Jin L, Zhao Q, Yuan M (2007) Arabidopsis MICROTUBULE-ASSOCIATED PROTEIN18 functions in directional cell growth by destabilizing cortical microtubules. Plant Cell 19:877–889PubMedCrossRefGoogle Scholar
  61. Wasteneys GO (2004) Progress in understanding the role of microtubules in plant cells. Curr Opin Plant Biol 7:651–660PubMedCrossRefGoogle Scholar
  62. Webb M, Jouannic S, Foreman J, Linstead P, Dolan L (2002) Cell specification in the Arabidopsis root epidermis requires the activity of ECTOPIC ROOT HAIR 3—a katanin-p60 protein. Development 129:123–131PubMedGoogle Scholar
  63. Whittington AT, Vugrek O, Wei KJ, Hasenbein NG, Sugimoto K, Rashnrooke MC, Wasteneys GO (2001) MOR1 is essential for organizing cortical microtubules in plant. Nature 411:610–613PubMedCrossRefGoogle Scholar
  64. Xu J, Scheres B (2005) Cell polarity: ROPing the ends together. Curr Opin Plant Biol 8:613–618PubMedCrossRefGoogle Scholar
  65. Yang Z, Fu Y (2007) ROP/RAC GTPase signaling. Curr Opin Plant Biol 10:490–494PubMedCrossRefGoogle Scholar
  66. Zelitch I (1961) Biochemical control of stomatal opening in leaves. Proc Natl Acad Sci USA 47:1423–1431PubMedCrossRefGoogle Scholar
  67. Zhang X, Dyachok J, Krishnakumar S, Smith LG, Oppenheimer DG (2005) IRREGULAR TRICHOME BRANCH1 in Arabidopsis encodes a plant homolog of the actin-related protien 2/3 complex activator SCAR/WAVE that regulates actin and microtubule organization. Plant Cell 17:2314–2326PubMedCrossRefGoogle Scholar
  68. Zhang C, Mallery EL, Schlueter J, Huang S, Fan Y, Brankle S, Staiger CJ, Szymanskia DB (2008) Arabidopsis SCARs function interchangeably to meet actin-related protein 2/3 activation thresholds during morphogenesis. Plant Cell 20:955–1011Google Scholar
  69. Zimmermann I, Saedler R, Mutondo M, Hulskamp M (2004) The Arabidopsis GNARLED gene encodes the NAP125 homolog and controls several actin-based cell shape changes. Mol Genet Genom 272:290–296CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  1. 1.Key Laboratory of Arid and Grassland Ecology, Ministry of Education, School of Life ScienceLanzhou UniversityGansuChina

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