Spatial control of cell expansion by the plant cytoskeleton

Annual Review of Cell and Developmental Biology

Volumn 21, Issue , 2005, Pages 271-295

  Smith, Laurie G ^a   Oppenheimer, David G ^b  

^a SECTION OF CELL AND DEVELOPMENTAL BIOLOGY   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

Author keywords

Actin; Microtubules; Morphogenesis; Tip growth; Trichomes

Indexed keywords

ACTIN; ACTIN RELATED PROTEIN 2; ACTIN RELATED PROTEIN 3; CALCIUM ION; CELLULOSE; F ACTIN; GUANOSINE TRIPHOSPHATASE;

CALCIUM TRANSPORT; CELL EXPANSION; CELL FUNCTION; CELL GROWTH; CELL SHAPE; CELL WALL; CYTOSKELETON; DYNAMICS; GOLGI COMPLEX; MICROTUBULE; MORPHOGENESIS; NONHUMAN; PLANT CELL; PLANT GROWTH; POLLEN TUBE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; TRICHOME;

CYTOSKELETON; MICROTUBULES; MODELS, BIOLOGICAL; MORPHOGENESIS; PLANTS;

EID: 26844554009     PISSN: 10810706     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.cellbio.21.122303.114901     Document Type: Review

References (112)

1. Baluska F, Jasik J, Edelmann HG, Salajova T, Volkmann D. 2001. Latrunculin B-induced dwarfism: plant cell elongation is F-actin-dependent. Dev. Biol. 231:113-24
2. Baskin TI. 2001. On the alignment of cellulose microfibrils by cortical microtubules: a review and a model. Protoplasma 215:150-71
3. Baskin TI, Bivens NJ. 1995. Stimulation of radial expansion in Arabidopsis roots by inhibitors of actomyosin and vesicle secretion but not by various inhibitors of metabolism. Planta 197:514-21
4. Basu D, El-Assal SE, Le J, Mallery EL, Szymanski DB. 2004. Interchangeable functions of Arabidopsis PIROGI and the human WAVE complex subunit SRA1 during leaf epidermal development. Development 131:4345-55
5. Basu D, Le J, El-Assal SE, Huang S, Zhang C, et al. 2005. DISTORTED3/SCAR2 is a putative Arabidopsis WAVE complex subunit that activates the Arp2/3 complex and is required for epidermal morphogenesis. Plant Cell 17:502-24
6. Brembu T, Winge P, Seem M, Bones AM. 2004. NAPP and PIRP encode subunits of a putative WAVE regulatory protein complex involved in plant cell morphogenesis. Plant Cell 16:2335-49
7. Brugnera E, Haney L, Grimsley C, Lu M, Walk SF, et al. 2002. Unconventional Rac-GEF activity is mediated through the Dock180-ELMO complex. Nat. Cell Biol. 4:574-82
8. Campbell P, Braam J. 1998. Co- and/or post-translational modifications are critical for TCH4 XET activity. Plant J. 15:553-61
9. Chen CY, Cheung AY, Wu HM. 2003. Actin-depolymerizing factor mediates Rac/Rop GTPase-regulated pollen tube growth. Plant Cell 15:237-49
10. Cheung AY, Wu HM. 2004. Overexpression of an Arabidopsis formin stimulates actin cable formation from pollen tube cell membrane. Plant Cell 16:257-69
11. Deeks MJ, Hussey PJ, Davies B. 2002. Formins: intermediates in signal-transduction cascades that affect cytoskeletal reorganization. Trends Plant Sci. 7:492-98
12. Deeks MJ, Kaloriti D, Davies B, Malho R, Hussey PJ. 2004. Arabidopsis NAP1 is essential for Arp2/3-dependent trichome morphogenesis. Curr. Biol. 14:1410-14
13. De Matteis MA, Di Girolamo M, Colanzi A, Pallas M, Di Tullio G, et al. 1994. Stimulation of endogenous ADP-ribosylation by brefeldin A. Proc. Natl. Acad. Sci. USA 91:1114-18
14. Dong C-H, Xia G-X, Hong Y, Ramachandran S, Kost B, Chua N-H. 2001. ADF proteins are involved in the control of flowering and regulate F-actin organization, cell expansion, and organ growth in Arabidopsis. Plant Cell 13:1333-46
15. Eden S, Rohtagi R, Podtelejnikov AV, Mann M, Kirschner M. 2002. Mechanism of regulation of WAVE1-induced actin nucleation by Rac1 and Nek. Nature 418:790-93
16. El-Assal SE, Le J, Basu D, Mallery EL, Szymanski DB. 2004a. Arabidopsis GNARLED encodes a NAP125 homolog that positively regulates Arp2/3. Curr. Biol. 14:1405-9
17. El-Assal SE, Le J, Basu D, Mallery EL, Szymanski DB. 2004b. DISTORTED2 encodes an ARPC2 subunit of the putative Arabidopsis ARP2/3 complex. Plant J. 38:526-38
18. Fisher DD, Cyr RJ. 1998. Extending the microtubule/microfibril paradigm: cellulose synthesis is required for normal cortical microtubule alignment in elongating cells. Plant Physiol. 116:1043-51
19. Fleming AJ, McQueen-Mason S, Mandel T, Kuhlemeier C. 1997. Induction of leaf primordia by the cell wall protein expansin. Science 276:1415-18
20. Folkers U, Berger J, Hülskamp M. 1997. Cell morphogenesis of trichomes in Arabidopsis: differential control of primary and secondary branching by branch initiation regulators and cell growth. Development 124:3779-86
21. Folkers U, Kirik V, Schobinger U, Falk S, Krishnakumar S, et al. 2002. The cell morphogenesis gene ANGUSTIFOLIA encodes a CtBP/BARS-like protein and is involved in the control of the microtubule cytoskeleton. EMBO J. 21:1280-88
22. Foreman J, Demidchik V, Bothwell JHF, Mylona P, Miedema H, et al. 2003. Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422:442-46
23. Frank M, Egile C, Dyachok J, Djakovic S, Nolasco M, et al. 2004. Activation of Arp2/3 complex-dependent actin polymerization by plant proteins distantly related to Scar/WAVE. Proc. Nat. Acad. Sci. USA 101:16379-84
24. Frank MJ, Cartwright HN, Smith LG. 2003. Three Brick genes have distinct functions in a common pathway promoting polarized cell division and cell morphogenesis in the maize leaf epidermis. Development 130:753-62
25. 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. 12:849-53
26. 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
27. 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 14:777-94
28. Fu Y, Wu G, Yang Z. 2001. Rop GTPase-dependent dynamics of tip-localized F-actin controls tip growth in pollen tubes. J. Cell Biol. 152:1019-32
29. Gautreau A, Ho HY, Steen H, Gygi SP, Kirschner MW. 2004. Purification and architecture of the ubiquitous WAVE complex. Proc. Natl. Acad. Sci. USA 101:4379-83
30. Geitmann A, Emons AMC. 2000. The cytoskeleton in plant and fungal cell tip growth. J. Microsc. 198:218-45
31. Geitmann A, Li YQ, Cresti M. 1996. The role of the cytoskeleton and dictyosome activity in the pulsatory growth of Nicotiana tabacum and Petunia hybrida pollen tubes. Bot. Acta 109:102-9
32. Gibbon BC, Kovar DR, Staiger CJ. 1999. Latrunculin B has different effects on pollen germination and tube growth. Plant Cell 11:2349-63
33. Giddings THJ, Staehelin LA. 1991. Microtubule-mediated control of microfibril deposition: a re-examination of the hypothesis. In The Cytoskeletal Basis of Plant Growth and Form, ed. CW Lloyd, pp. 85-99. New York: Academic
34. Gilliland LU, Kandasamy MK, Pawloski LC, Meagher RB. 2002. Both vegetative and reproductive actin isovariants complement the stunted root hair phenotype of the Arabidopsis act 2-1 mutation. Plant Physiol. 130:2199-209
35. Gu Y, Fu Y, Dowd P, Li S, Vernoud V, et al. 2005. A Rho-family GTPase controls actin dynamics and tip growth via two counteracting downstream pathways in pollen tubes. J. Cell Biol. 169:127-38
36. Gu Y, Wang Z, Yang Z. 2004. ROP/RAC GTPase: an old new master regulator for plant signaling. Curr. Opin. Plant Biol. 7:527-36
37. Hepler PK, Vidali L, Cheung AY. 2001. Polarized cell growth in higher plants. Annu. Rev. Cell Dev. Biol. 17:159-87
38. Higgs HN, Pollard TD. 2001. Regulation of actin filament network formation through the Arp2/3 complex: activation by a diverse array of proteins. Annu. Rev. Biochem. 70:649-76
39. Holdaway-Clarke TL, Hepler PK. 2003. Control of pollen tube growth: role of ion gradients and fluxes. New Phytol. 159:539-63
40. Holweg C, Nick P. 2004. Arabidopsis myosin XI mutant is defective in organelle movement and polar auxin transport. Proc. Nat. Acad. Sci. USA 101:10488-93
41. Huang S, Blanchoin L, Chaudhry F, Franklin-Tong VE, Staiger CJ. 2004. A gelsolin-like protein from Papaver rhoeas pollen (PrABPSO) stimulates calcium-regulated severing and depolymerization of actin filaments. J. Biol. Chem. 279:23364-75
42. Hülskamp M. 2000. How plants split hairs. Curr. Biol. 10:R308-10
43. Hülskamp M, Miséra S, Jürgens G. 1994. Genetic dissection of trichome cell development in Arabidopsis. Cell 76:555-66
44. Innocenti M, Zucconi A, Disanza A, Frittoli E, Areces L, et al. 2004. Abi1 is essential for the formation and activation of a WAVE2 signaling complex mediating Rac-dependent actin remodeling. Nat. Cell Biol. 6:319-27
45. Jones MA, Shen J-J, Fu Y, Li H, Yang Z, Grierson CS. 2002. The Arabidopsis Rop2 GTPase is a positive regulator of both root hair initiation and tip growth. Plant Cell 14:763-76
46. Ketelaar T, Allwood EG, Anthony R, Voigt B, Menzel D, Hussey PJ. 2004. The actin-interacting protein AIP1 is essential for actin organization and plant development. Curr. Biol. 14:145-49
47. Ketelaar T, de Ruijter NCA, Emons AMC. 2003. Unstable F-actin specifies the area and microtubule direction of cell expansion in Arabidopsis root hairs. Plant Cell 15:285-92
48. Ketelaar T, Emons AMC. 2001. The cytoskeleton in plant cell growth: lessons from root hairs. New Phytol. 152:409-18
49. Ketelaar T, Faivre-Moskalenko C, Esseling JJ, de Ruijter NCA, Grierson CS, et al. 2002. Positioning of nuclei in Arabidopsis root hairs: an actin-regulated process of tip growth. Plant Cell 14:2941-55
50. Kim GT, Shoda K, Tsuge T, Cho KH, Uchimiya H, et al. 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. 21:1267-79
51. Kost B, Spielhofer P, Chua NH. 1998. A GFP-mouse talin fusion protein labels plant actin filaments in vivo and visualizes the actin cytoskeleton in growing pollen tubes. Plant J. 16:393-401
52. Kovar DR, Drøbak BK, Staiger CJ. 2000. Maize profilin isoforms are functionally distinct. Plant Cell 12:583-98
53. Lang T, Wacker I, Wunderlich I, Rohrbach A, Giese G, et al. 2000. Role of actin cortex in the subplasmalemmal transport of secretory granules in PC-12 cells. Biophys. J. 78:2863-77
54. Le J, El-Assal SE, Basu D, Saad ME, Szymanski DB. 2003. Requirements for Arabidopsis ATARP2 and ATARP3 during epidermal development. Curr. Biol. 13:1341-47
55. Li H, Lin Y, Heath RM, Zhu MX, Yang Z. 1999. Control of pollen tube tip growth by a Rop GTPase-dependent pathway that leads to tip-localized calcium influx. Plant Cell 11:1731-42
56. Li S, Blanchoin L, Yang Z, Lord EM. 2003. The putative Arabidopsis Arp2/3 complex controls leaf cell morphogenesis. Plant Physiol. 132:2034-44
57. Li Y, Sorefan K, Hemmann G, Bevan MW. 2004. Arabidopsis NAP and PIR regulate actin-based cell morphogenesis and multiple developmental processes. Plant Physiol. 136:3616-27
58. Lin Y, Wang Y, Zhu J-K, Yang Z. 1996. Localization of a Rho GTPase implies a role in tip growth and movement of the generative cell in pollen tubes. Plant Cell 8:293-303
59. Lin Y, Yang Z. 1997. Inhibition of pollen tube elongation by microinjected anti-Rop1 antibodies suggests a crucial role for Rho-type GTPases in the control of tip growth. Plant Cell 9:1647-59
60. Lloyd CW, Chan J. 2004. Microtubules and the shape of plants to come. Nat. Rev. Mol. Cell Biol. 5:13-22
61. Lu L, Lee YR, Pan R, Maloof JN, Liu B. 2005. An internal motor kinesin is associated with the Golgi apparatus and plays a role in trichome morphogenesis in Arabidopsis. Mol. Biol. Cell 16:811-23
62. Luo D, Oppenheimer DG. 1999. Genetic control of trichome branch number in Arabidopsis: the roles of the FURCA loci. Development 126:5547-57
63. Marks MD, Esch J, Herman P, Sivakumaran S, Oppenheimer D. 1991. A model for cell-type determination and differentiation in plants. In Molecular Biology of Plant Development, ed. G Jenkins, W Schuch, pp. 259-75. Cambridge, UK: Co. Biol. Ltd.
64. Mathur J. 2004. Cell shape development in plants. Trends Plant Sci. 9:583-90
65. Mathur J, Chua N-H. 2000. Microtubule stabilization leads to growth reorientation in Arabidopsis trichomes. Plant Cell 12:465-77
66. Mathur J, Spielhofer P, Kost B, Chua N. 1999. The actin cytoskeleton is required to elaborate and maintain spatial patterning during trichome cell morphogenesis in Arabidopsis thaliana. Development 126:5559-68
67. Mathur J, Mathur N, Kernebeck B, Hülskamp M. 2003a. Mutations in actin-related proteins 2 and 3 affect cell shape development in Arabidopsis. Plant Cell 15:1632-45
68. Mathur J, Mathur N, Kirik V, Kernebeck B, Srinivas BP, Hülskamp 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 130:3137-46
69. McKinney EC, Kandasamy MK, Meagher RB. 2001. Small changes in the regulation of one Arabidopsis profilin isovariant, PRF1, alter seedling development. Plant Cell 13:1179-91
70. Meller N, Irani-Tehrani M, Kiosses WB, Del Pozo MA, Schwartz MA. 2002. Zizimin1, a novel Cdc42 activator, reveals a new GEF domain for Rho proteins. Nat. Cell Biol. 4:639-47
71. Miller DD, de Ruijter NCA, Bisseling T, Emons AMC. 1999. The role of actin in root hair morphogenesis: studies with lipochito-oligosaccharide as a growth stimulator and cytochalasin as an actin perturbing drug. Plant J. 17:141-54
72. Miller DD, Lancelle SA, Hepler PK. 1996. Actin microfilaments do not form a dense meshwork in Lilium longiflorum pollen tube tips. Protoplasma 195:123-32
73. Molendijk A, Bischoff F, Rajendrakumar CSV, Friml J, Braun M, et al. 2001. Arabidopsis thaliana Rop GTPases are localized to tips of root hairs and control polar growth. EMBO J. 20:2779-88
74. Nardini M, Spano S, Cericola C, Pesce A, Massaro A, et al. 2003. CtBP/BARS: a dual-function protein involved in transcription co-repression and Golgi membrane fission. EMBO J. 22:3122-30
75. Nebenführ A, Gallagher LA, Dunahay TG, Frohlick JA, Mazurkiewicz AM, et al. 1999. Stop-and-go movements of plant Golgi stacks are mediated by the acto-myosin system. Plant Physiol. 121:1127-42
76. Oppenheimer DG, Pollock MA, Vacik J, Szymanski DB, Ericson B, et al. 1997. Essential role of a kinesin-like protein in Arabidopsis trichome morphogenesis. Proc. Nat. Acad. Sci. USA 94:6261-66
77. 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 14:101-18
78. Pien S, Wyrzykowska J, McQueen-Mason S, Smart C, Fleming A. 2001. Local expression of expansin induces the entire process of leaf development and modifies leaf shape. Proc. Nat. Acad. Sci. USA 98:11812-17
79. Pollard TD, Borisy GG. 2003. Cellular motility driven by assembly and disassembly of actin filaments. Cell 112:453-65
80. Ramachandran S, Christensen HEM, Ishimaru Y, Dong C-H, Chao-Ming W, et al. 2000. Profilin plays a role in cell elongation, cell shape maintenance, and flowering in Arabidopsis. Plant Physiol. 124:1637-47
81. Reddy AS, Day IS. 2000. The role of the cytoskeleton and a molecular motor in trichome morphogenesis. Trends Plant Sci. 5:503-5
82. Reddy AS, Day IS. 2001. Kinesins in the Arabidopsis genome: a comparative analysis among eukaryotes. BMC Genomics 2:2
83. Reddy ASN, Narasimhulu SB, Safadi F, Golovkin M. 1996a. A plant kinesin heavy chain-like protein is a calmodulin-binding protein. Plant J. 10:9-21
84. Reddy ASN, Safadi F, Narasimhulu SB, Golovkin M, Hu X. 1996b. A novel plant calmodulin-binding protein with a kinesin heavy chain motor domain. J. Biol. Chem. 271:7052-60
85. Reddy VS, Reddy AS. 1999. A plant calmodulin-binding motor is part kinesin and part myosin. Bioinformatics 15:1055-57
86. Rédei GP. 1962. Single locus heterosis. Z. Vererbungsl. 93:164-70
87. Rose JK, Braam J, Fry SC, Nishitani K. 2002. The XTH family of enzymes involved in xyloglucan endotransglucosylation and endohydrolysis: current perspectives and a new unifying nomenclature. Plant Cell Physiol. 43:1421-35
88. Saedler R, Mathur N, Srinivas BP, Kernebeck B, Hülskamp M, Mathur J. 2004. Actin control over microtubules suggested by DISTORTED2 encoding the Arabidopsis ARPC2 subunit homolog. Plant Cell Physiol. 45:813-22
89. Schaeper U, Subramanian T, Lim L, Boyd JM, Chinnadurai G. 1998. Interaction between a cellular protein that binds to the C-terminal region of adenovirus E1A (CtBP) and a novel cellular protein is disrupted by E1A through a conserved PLDLS motif. J. Biol. Chem. 273:8549-52
90. Schwab B, Mathur J, Saedler R, Schwarz H, Frey B, et al. 2003. Regulation of cell expansion by the DISTORTED genes in Arabidopsis thaliana: actin controls the spatial organization of microtubules. Mol. Genet. Genomics 269:350-60
91. Smith LG. 2003. Cytoskeletal control of plant cell shape: getting the fine points. Curr. Opin. Plant Biol. 6:63-73
92. Spano S, Silletta MG, Colanzi A, Alberti S, Fiucci G, et al. 1999. Molecular cloning and functional characterization of brefeldin A-ADP-ribosylated substrate. A novel protein involved in the maintenance of the Golgi structure. J. Biol. Chem. 274:17705-10
93. Steffen A, Rottner K, Ehinger J, Innocenti M, Seita G, et al. 2004. Sra-1 and Nap1 link Rac to actin assembly driving lamellipodia formation. EMBO J. 23:749-59
94. Sugimoto K, Himmelspach R, Williamson RE, Wasteneys GO. 2003. Mutation or drug-dependent microtubule disruption causes radial swelling without altering parallel cellulose microfibril deposition in Arabidopsis root cells. Plant Cell 15:1414-29
95. Szymanski DB. 2005. Breaking the WAVE complex: the point of Arabidopsis trichomes. Curr. Opin. Plant Biol. 8:103-112
96. Szymanski DB, Marks MD, Wick SM. 1999. Organized F-actin is essential for normal trichome morphogenesis in Arabidopsis. Plant Cell 11:2331-47
97. Thimann KV, Reese K, Nachmias VT. 1992. Actin and the elongation of plant cells. Protoplasma 171:153-66
98. Tsuge T, Tsukaya H, Uchimiya H. 1996. Two independent and polarized processes of cell elongation regulate leaf blade expansion in Arabidopsis thaliana (L.) Heynh. Development 122:1589-600
99. Vidali L, McKenna ST, Hepler PK. 2001. Actin polymerization is essential for pollen tube growth. Mol. Biol. Cell 12:2534-45
100. Vissenberg K, Fry SC, Pauly M, Höfte H, Verbelen JP. 2005. XTH acts at the microfibril-matrix interface during cell elongation. J. Exp. Bot. 56:673-83
101. Vissenberg K, Fry SC, Verbelen JP. 2001. Root hair initiation is coupled to a highly localized increase of xyloglucan endotransglycosylase action in Arabidopsis roots. Plant Physiol. 127:1125-35
102. 2+-permeable channels in the plasma membrane of Arabidopsis pollen are regulated by actin microfilaments. Plant Physiol. 136:3892-904
103. Wang Y-S, Motes CM, Mohamalawari DR, Blancaflor EB. 2004. Green fluorescent protein fusions to Arabidopsis Fimbrin 1 for spatio-temporal imaging of F-actin dynamics in roots. Cell Motil. Cytoskel. 59:79-93
104. Wasteneys GO. 2004. Progress in understanding the role of microtubules in plant cells. Curr. Opin. Plant Biol. 7:651-60
105. Wasteneys GO, Galway ME. 2003. Remodeling the cytoskeleton for growth and form: an overview with some new views. Annu. Rev. Plant Biol. 54:691-722
106. Wasteneys GO, Yang Z. 2004. New views on the plant cytoskeleton. Plant Physiol. 136:3884-91
107. Weigert R, Silletta MG, Spano S, Turacchio G, Cericola C, et al. 1999. CtBP/BARS induces fission of Golgi membranes by acylating lysophosphatidic acid. Nature 402:429-33
108. Whittington AT, Vugrek O, Wei KJ, Hasenbein NG, Sugimoto K, et al. 2001. MOR1 is essential for organizing cortical microtubules in plants. Nature 411:610-13
109. Zhang X, Dyachok J, Krishnakumar S, Smith LG, Oppenheimer DG. 2005b. The Arabidopsis IRREGULAR TRICHOME BRANCH 1 (ITB1) gene encodes a plant homolog of the Arp2/3 complex activator Scar/WAVE that regulates actin and microtubule organization. Plant Cell. In press
110. Zhang X, Grey PH, Krishnakumar S, Oppenheimer DG. 2005a. The IRREGULAR TRICHOME BRANCH loci regulate trichome elongation in Arabidopsis. Plant Cell Physiol. 17:1-13
111. Zhong R, Burk DH, Morrison WH 3rd, Ye ZH. 2002. A kinesin-like protein is essential for oriented deposition of cellulose microfibrils and cell wall strength. Plant Cell 14:3101-17
112. Zimmermann I, Saedler R, Mutondo M, Hülskamp M. 2004. The Arabidopsis GNARLED gene encodes the NAP125 homolog and controls several actin-based cell shape changes. Mol. Genet. Genomics 272:290-96