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Molecular mechanisms controlling pavement cell shape in Arabidopsis leaves

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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.

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References

  • 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 131:4345–4355

    Article  PubMed  CAS  Google Scholar 

  • 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 17:502–524

    Article  PubMed  Google Scholar 

  • 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 105:4044–4049

    Article  PubMed  CAS  Google Scholar 

  • 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 25:137–148

    Article  PubMed  CAS  Google Scholar 

  • 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 404:1007–1011

    Article  PubMed  CAS  Google Scholar 

  • 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 116:791–801

    Article  PubMed  CAS  Google Scholar 

  • 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 14:2577–2590

    Article  PubMed  CAS  Google Scholar 

  • 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 13:807–827

    Article  PubMed  CAS  Google Scholar 

  • 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 438:1013–1016

    Article  PubMed  CAS  Google Scholar 

  • 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 146:97–107

    Article  PubMed  CAS  Google Scholar 

  • Chisholm AD, Hardin J (2005) Epidermal morphogenesis. In: WormBook. The C. elegans Research Community

  • Cooper JA, Wear MA, Weaver AM (2001) Arp2/3 complex: advances on the inner workings of a molecular machine. Cell 107:703–705

    Article  PubMed  CAS  Google Scholar 

  • Deeks MJ, Hussey PJ (2003) ARP2/3 and ‘The shape of things to come’. Curr Opin Plant Biol 6:257–269

    Article  Google Scholar 

  • Deeks MJ, Kaloriti D, Davies B, Malho R, Hussey PJ (2004) Arabidopsis NAP1 is essential for Arp2/3-dependent trichome morphogenesis. Curr Biol 14:1410–1414

    Article  PubMed  CAS  Google Scholar 

  • 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 133:1091–1100

    Article  PubMed  CAS  Google Scholar 

  • 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 165:1227–1237

    Article  PubMed  CAS  Google Scholar 

  • 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 14:1405–1409

    Article  Google Scholar 

  • 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 38:526–538

    Article  Google Scholar 

  • 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 130:4011–4024

    Article  PubMed  CAS  Google Scholar 

  • 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 21:1280–1288

    Article  Google Scholar 

  • 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 12:849–853

    Article  PubMed  CAS  Google Scholar 

  • 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 101:16379–16384

    Article  PubMed  CAS  Google Scholar 

  • 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 14:777–794

    Article  PubMed  CAS  Google Scholar 

  • 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 120:687–700

    Article  PubMed  CAS  Google Scholar 

  • 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 12:2075–2086

    Article  PubMed  CAS  Google Scholar 

  • Guimil S, Dunand C (2007) Cell growth and differentiation in Arabidopsis epidermal cell. J Exp Bot 14:3829–3840

    Article  Google Scholar 

  • 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 70:649–676

    Article  PubMed  CAS  Google Scholar 

  • Horanic GE, Gardner FE (1967) An improved method of making epidermal imprints. Bot Gaz 128:144–150

    Article  Google Scholar 

  • Hulskamp M, Misera S, Jurgens G (1994) Genetic dissection of trichome cell development in Arabidopsis. Cell 76:555–566

    Article  PubMed  CAS  Google Scholar 

  • Jaffe AB, Hall A (2005) Rho GTPases: biochemistry and biology. Annu Rev Cell Dev Biol 21:247–269

    Article  PubMed  CAS  Google Scholar 

  • 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 21:1267–1279

    Article  PubMed  CAS  Google Scholar 

  • 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 11:1891–1895

    Article  PubMed  CAS  Google Scholar 

  • Kotzer AM, Wasteneys GO (2006) Mechanisms behind the puzzle: microtubule–microfilament cross-talk in pavement cell formation. Can J Bot 84:594–603

    Article  CAS  Google Scholar 

  • 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 17:947–952

    Article  PubMed  CAS  Google Scholar 

  • Le J, El-Assal SE, Basu D, Saad ME, Szymanksi DB (2003) Requirements for Arabidopsis ATARP2 and ATARP3 during epidermal development. Curr Biol 13:1341–1347

    Article  PubMed  CAS  Google Scholar 

  • Lew DJ (2003) The morphogenesis checkpoint: how yeast cells watch their figures. Curr Opin Cell Biol 15:648–653

    Article  PubMed  CAS  Google Scholar 

  • Li H, Shen J, Zheng Z, Lin Y, Yang Z (2001) The Rop GTPase switch controls multiple developmental processes in Arabidopsis. Plant Physiol 126:670–684

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Li Y, Sorefan K, Hemmann G, Bevan MW (2004) Arabidopsis NAP and PIR regulate actin-based cell morphogenesis and multiple developmental processes. Plant Physiol 136:3616–3627

    Article  PubMed  CAS  Google Scholar 

  • Mathur J (2006) Local interactions shape plant cell. Curr Opin Cell Biol 18:40–46

    Article  PubMed  CAS  Google Scholar 

  • Mathur J, Koncz C (1997) Method for preparation of epidermal imprints using agarose. Biotechnology 22:280–282

    CAS  Google Scholar 

  • 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 126:5559–5568

    PubMed  CAS  Google Scholar 

  • 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 15:1632–1645

    Article  PubMed  CAS  Google Scholar 

  • 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 130:3137–3146

    Article  PubMed  CAS  Google Scholar 

  • McClinton RS, Chandler JS, Callis J (2001) cDNA isolation, characterization, and protein intracellular localization of a katanin-like p60 subunit from Arabidopsis thaliana. Protoplasma 216:181–190

    Article  PubMed  CAS  Google Scholar 

  • 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 95:6181–6186

    Article  PubMed  CAS  Google Scholar 

  • 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 167:721–732

    Article  PubMed  CAS  Google Scholar 

  • Panteris E, Apostolakos P, Galatis B (1993) Microtubles and morphogenesis in ordinary epidermal cell of Vigna sinensis leaves. Protoplasma 174:91–100

    Article  Google Scholar 

  • Panteris E, Apostolakos P, Galatis B (1994) Sinuous ordinary epidermal cells—behind several patterns of waviness, a common morphogenetic mechanism. Protoplasma 127:771–780

    Google Scholar 

  • Parker JS, Cavell AC, Dolan L, Roberts K, Grierson CS (2000) Genetic interactions during root hair morphogenesis in Arabidopsis. Plant Cell 12:1961–1974

    Article  PubMed  CAS  Google Scholar 

  • 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 14:101–118

    Article  PubMed  CAS  Google Scholar 

  • 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 20:1470–1481

    Article  PubMed  CAS  Google Scholar 

  • Robinson RC, Turbedsky K, Kaiser DA, Marchand JB, Higgs HN, Choe S, Pollard TD (2001) Crystal structure of Arp2/3 complex. Science 294:1679–1684

    Article  PubMed  CAS  Google Scholar 

  • Sampson J (1961) A method of replicating dry or moist surfaces for examination by light microscopy. Nature 191:932–933

    Article  PubMed  CAS  Google Scholar 

  • 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 269:350–360

    Article  CAS  Google Scholar 

  • Smith LG, Oppenheimer DG (2005) Spatial control of cell expansion by the plant cytoskeleton. Annu Rev Cell Dev Biol 21:271–295

    Article  PubMed  CAS  Google Scholar 

  • 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 145:1009–1026

    Article  PubMed  CAS  Google Scholar 

  • Traas J, Hulskamp M, Gendreau E, Hofte H (1998) Endoreduplication and development: rule without dividing? Curr Opin Plant Biol 1:498–530

    Article  PubMed  CAS  Google Scholar 

  • 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 134:967–977

    Article  PubMed  CAS  Google Scholar 

  • 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 19:877–889

    Article  PubMed  CAS  Google Scholar 

  • Wasteneys GO (2004) Progress in understanding the role of microtubules in plant cells. Curr Opin Plant Biol 7:651–660

    Article  PubMed  CAS  Google Scholar 

  • 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 129:123–131

    PubMed  CAS  Google Scholar 

  • 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 411:610–613

    Article  PubMed  CAS  Google Scholar 

  • Xu J, Scheres B (2005) Cell polarity: ROPing the ends together. Curr Opin Plant Biol 8:613–618

    Article  PubMed  CAS  Google Scholar 

  • Yang Z, Fu Y (2007) ROP/RAC GTPase signaling. Curr Opin Plant Biol 10:490–494

    Article  PubMed  CAS  Google Scholar 

  • Zelitch I (1961) Biochemical control of stomatal opening in leaves. Proc Natl Acad Sci USA 47:1423–1431

    Article  PubMed  CAS  Google Scholar 

  • 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 17:2314–2326

    Article  PubMed  CAS  Google Scholar 

  • 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 20:955–1011

    Google Scholar 

  • 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 272:290–296

    Article  CAS  Google Scholar 

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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).

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  1. Key Laboratory of Arid and Grassland Ecology, Ministry of Education, School of Life Science, Lanzhou University, 730000, Gansu, China

    Pingping Qian, Suiwen Hou & Guangqin Guo

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  1. Pingping Qian
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  2. Suiwen Hou
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  3. Guangqin Guo
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Correspondence to Suiwen Hou.

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Communicated by R. Reski.

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Qian, P., Hou, S. & Guo, G. Molecular mechanisms controlling pavement cell shape in Arabidopsis leaves. Plant Cell Rep 28, 1147–1157 (2009). https://doi.org/10.1007/s00299-009-0729-8

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