Cytoskeleton and Root Hair Growth

Chapter
Part of the Advances in Plant Biology book series (AIPB, volume 2)

Abstract

Root hairs are long tubular outgrowths of root epidermis cell that form to increase the root surface in order to assist in the uptake of water and nutrients from soil. Root hair development consists of two distinct processes: root hair initiation and tip growth. During both events, the dynamic organization of the cytoskeleton translates local signaling events into a focused growth response that is critical during root hair growth. Microtubules are primarily important for maintenance of the direction of tip growth. The actin cytoskeleton, on the other hand, is crucial for the selection of the root hair initiation site and maintenance of tip growth. The unique cytoskeletal organization found in growing root hairs controls the polar delivery of membranes to the apex in order to enlarge the cell unidirectionally. Signaling factors, such as calcium and reactive oxygen species, are instrumental in maintaining polarity of the cytoskeleton, vesicle trafficking, and ultimately root hair growth. Interestingly, these regulatory factors are interdependent upon each other, so that an elaborate set of feedback loops forms that results in a stable self-organized cell polarity.

Keywords

Maize Germinate Cytosol Fluorescein Washout 

References

  1. 1.
    Avisar D, Abu-Abied M, Belausov E, Sadot E, Hawes C, Sparkes IA (2009) A comparative study of the involvement of 17 Arabidopsis myosin family members on the motility of Golgi and other organelles. Plant Physiol 150:700–709CrossRefPubMedGoogle Scholar
  2. 2.
    Baluska F, Salaj J, Mathur J, Braun M, Jasper F, Samaj J, Chua NH, Barlow PW, Volkmann D (2000) Root hair formation: F-actin-dependent tip growth is initiated by local assembly of profilin-supported F-actin meshworks accumulated within expansin-enriched bulges. Dev Biol 227:618–632CrossRefPubMedGoogle Scholar
  3. 3.
    Baluska F, Volkmann D (2002) Pictures in cell biology. Actin-driven polar growth of plant cells. Trends Cell Biol 12:14CrossRefPubMedGoogle Scholar
  4. 4.
    Baluska F, Wojtaszek P, Volkmann D, Barlow P (2003) The architecture of polarized cell growth: the unique status of elongating plant cells. Bioessays 25:569–576CrossRefPubMedGoogle Scholar
  5. 5.
    Bao Y, Kost B, Chua NH (2001) Reduced expression of alpha-tubulin genes in Arabidopsis thaliana specifically affects root growth and morphology, root hair development and root gravitropism. Plant J 28:145–157CrossRefPubMedGoogle Scholar
  6. 6.
    Baxter-Burrell A, Yang Z, Springer PS, Bailey-Serres J (2002) RopGAP4-dependent Rop GTPase rheostat control of Arabidopsis oxygen deprivation tolerance. Science 296:2026–2028CrossRefPubMedGoogle Scholar
  7. 7.
    Bibikova TN, Blancaflor EB, Gilroy S (1999) Microtubules regulate tip growth and orientation in root hairs of Arabidopsis thaliana. Plant J 17:657–665CrossRefPubMedGoogle Scholar
  8. 8.
    Bibikova TN, Jacob T, Dahse I, Gilroy S (1998) Localized changes in apoplastic and cytoplasmic pH are associated with root hair development in Arabidopsis thaliana. Development 125:2925–2934PubMedGoogle Scholar
  9. 9.
    Bibikova TN, Zhigilei A, Gilroy S (1997) Root hair growth in Arabidopsis thaliana is directed by calcium and an endogenous polarity. Planta 203:495–505CrossRefPubMedGoogle Scholar
  10. 10.
    Braun M, Baluska F, von Witsch M, Menzel D (1999) Redistribution of actin, profilin and phosphatidylinositol-4, 5-bisphosphate in growing and maturing root hairs. Planta 209:435–443CrossRefPubMedGoogle Scholar
  11. 11.
    Carol RJ, Dolan L (2002) Building a hair: tip growth in Arabidopsis thaliana root hairs. Philos Trans R Soc Lond B Biol Sci 357:815–821CrossRefPubMedGoogle Scholar
  12. 12.
    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 438:1013–1016CrossRefPubMedGoogle Scholar
  13. 13.
    Cole RA, Fowler JE (2006) Polarized growth: maintaining focus on the tip. Curr Opin Plant Biol 9:579–588CrossRefPubMedGoogle Scholar
  14. 14.
    Collings DA, Lill AW, Himmelspach R, Wasteneys GO (2006) Hypersensitivity to cytoskeletal antagonists demonstrates microtubule-microfilament cross-talk in the control of root elongation in Arabidopsis thaliana. New Phytol 170:275–290CrossRefPubMedGoogle Scholar
  15. 15.
    Deeks MJ, Cvrckova F, Machesky LM, Mikitova V, Ketelaar T, Zarsky V, Davies B, Hussey PJ (2005) Arabidopsis group Ie formins localize to specific cell membrane domains, interact with actin-binding proteins and cause defects in cell expansion upon aberrant expression. New Phytol 168:529–540CrossRefPubMedGoogle Scholar
  16. 16.
    Dolan L, Costa S (2001) Evolution and genetics of root hair stripes in the root epidermis. J Exp Bot 52:413–417PubMedGoogle Scholar
  17. 17.
    Era A, Tominaga M, Ebine K, Awai C, Saito C, Ishizaki K, Yamato KT, Kohchi T, Nakano A, Ueda T (2009) Application of Lifeact reveals F-actin dynamics in Arabidopsis thaliana and the liverwort, Marchantia polymorpha. Plant Cell Physiol 50:1041–1048CrossRefPubMedGoogle Scholar
  18. 18.
    Felle HH, Hepler PK (1997) The Cytosolic Ca2+ Concentration Gradient of Sinapis alba Root Hairs as Revealed by Ca2+-Selective Microelectrode Tests and Fura-Dextran Ratio Imaging. Plant Physiol 114:39–45PubMedGoogle Scholar
  19. 19.
    Fischer U, Ikeda Y, Grebe M (2007) Planar polarity of root hair positioning in Arabidopsis. Biochem Soc Trans 35:149–151CrossRefPubMedGoogle Scholar
  20. 20.
    Foreman J, Demidchik V, Bothwell JH, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones JD, Davies JM, Dolan L (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422:442–446CrossRefPubMedGoogle Scholar
  21. 21.
    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 14:777–794CrossRefPubMedGoogle Scholar
  22. 22.
    Geitmann A, Emons AM (2000) The cytoskeleton in plant and fungal cell tip growth. J Microsc 198:218–245CrossRefPubMedGoogle Scholar
  23. 23.
    Gilliland LU, Kandasamy MK, Pawloski LC, Meagher RB (2002) Both vegetative and reproductive actin isovariants complement the stunted root hair phenotype of the Arabidopsis act2-1 mutation. Plant Physiol 130:2199–2209CrossRefPubMedGoogle Scholar
  24. 24.
    Grebe M (2004) Ups and downs of tissue and planar polarity in plants. Bioessays 26:719–729CrossRefPubMedGoogle Scholar
  25. 25.
    Grebe M, Friml J, Swarup R, Ljung K, Sandberg G, Terlou M, Palme K, Bennett MJ, Scheres B (2002) Cell polarity signaling in Arabidopsis involves a BFA-sensitive auxin influx pathway. Curr Biol 12:329–334CrossRefPubMedGoogle Scholar
  26. 26.
    Guimil S, Dunand C (2007) Cell growth and differentiation in Arabidopsis epidermal cells. J Exp Bot 58:3829–3840CrossRefPubMedGoogle Scholar
  27. 27.
    He X, Liu YM, Wang W, Li Y (2006) Distribution of G-actin is related to root hair growth of wheat. Ann Bot 98:49–55CrossRefPubMedGoogle Scholar
  28. 28.
    Hemsley PA, Kemp AC, Grierson CS (2005) The TIP GROWTH DEFECTIVE1 S-acyl transferase regulates plant cell growth in Arabidopsis. Plant Cell 17:2554–2563CrossRefPubMedGoogle Scholar
  29. 29.
    Hepler PK, Vidali L, Cheung AY (2001) Polarized cell growth in higher plants. Annu Rev Cell Dev Biol 17:159–187CrossRefPubMedGoogle Scholar
  30. 30.
    Hussey, P.J., T. Ketelaar, and M.J. Deeks (2006) Control of the actin cytoskeleton in plant cell growth. Annu Rev Plant Biol. 57:109–125Google Scholar
  31. 31.
    Ishida T, Kurata T, Okada K, Wada T (2008) A genetic regulatory network in the development of trichomes and root hairs. Annu Rev Plant Biol 59:365–386CrossRefPubMedGoogle Scholar
  32. 32.
    Kandasamy MK, McKinney EC, Meagher RB (2009) A single vegetative actin isovariant overexpressed under the control of multiple regulatory sequences is sufficient for normal Arabidopsis development. Plant Cell 21:701–718CrossRefPubMedGoogle Scholar
  33. 33.
    Ketelaar T, Allwood EG, Hussey PJ (2007) Actin organization and root hair development are disrupted by ethanol-induced overexpression of Arabidopsis actin interacting protein 1 (AIP1). New Phytol 174:57–62CrossRefPubMedGoogle Scholar
  34. 34.
    Ketelaar T, Anthony RG, Hussey PJ (2004) Green fluorescent protein-mTalin causes defects in actin organization and cell expansion in Arabidopsis and inhibits actin depolymerizing factor’s actin depolymerizing activity in vitro. Plant Physiol 136:3990–3998CrossRefPubMedGoogle Scholar
  35. 35.
    Kovar DR, Drobak BK, Staiger CJ (2000) Maize profilin isoforms are functionally distinct. Plant Cell 12:583–598CrossRefPubMedGoogle Scholar
  36. 36.
    Li JF, Nebenführ A (2007) Organelle targeting of myosin XI is mediated by two globular tail subdomains with separate cargo binding sites. J Biol Chem 282:20593–20602CrossRefPubMedGoogle Scholar
  37. 37.
    Lloyd CW, Wells B (1985) Microtubules are at the tips of root hairs and form helical patterns corresponding to inner wall fibrils. J Cell Sci 75:225–238PubMedGoogle Scholar
  38. 38.
    Masucci JD, Schiefelbein JW (1994) The rhd6 Mutation of Arabidopsis thaliana Alters Root-Hair Initiation through an Auxin- and Ethylene-Associated Process. Plant Physiol 106:1335–1346PubMedGoogle Scholar
  39. 39.
    Miller D, de Ruijter NC, Bisseling T, Emons AM (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 17:141–154CrossRefGoogle Scholar
  40. 40.
    Molendijk AJ, Bischoff F, Rajendrakumar CS, Friml J, Braun M, Gilroy S, Palme K (2001) Arabidopsis thaliana Rop GTPases are localized to tips of root hairs and control polar growth. EMBO J 20:2779–2788CrossRefPubMedGoogle Scholar
  41. 41.
    Monshausen GB, Bibikova TN, Messerli MA, Shi C, Gilroy S (2007) Oscillations in extracellular pH and reactive oxygen species modulate tip growth of Arabidopsis root hairs. Proc Natl Acad Sci USA 104:20996–21001CrossRefPubMedGoogle Scholar
  42. 42.
    Monshausen GB, Messerli MA, Gilroy S (2008) Imaging of the Yellow Cameleon 3.6 indicator reveals that elevations in cytosolic Ca2+ follow oscillating increases in growth in root hairs of Arabidopsis. Plant Physiol 147:1690–1698CrossRefPubMedGoogle Scholar
  43. 43.
    Ojangu EL, Jarve K, Paves H, Truve E (2007) Arabidopsis thaliana myosin XIK is involved in root hair as well as trichome morphogenesis on stems and leaves. Protoplasma 230:193–202CrossRefPubMedGoogle Scholar
  44. 44.
    Ovecka M, Lang I, Baluska F, Ismail A, Illes P, Lichtscheidl IK (2005) Endocytosis and vesicle trafficking during tip growth of root hairs. Protoplasma 226:39–54CrossRefPubMedGoogle Scholar
  45. 45.
    Payne RJ, Grierson CS (2009) A theoretical model for ROP localisation by auxin in Arabidopsis root hair cells. PLoS ONE 4:e8337CrossRefPubMedGoogle Scholar
  46. 46.
    Peremyslov VV, Prokhnevsky AI, Avisar D, Dolja VV (2008) Two class XI myosins function in organelle trafficking and root hair development in Arabidopsis. Plant Physiol 146:1109–1116CrossRefPubMedGoogle Scholar
  47. 47.
    Preuss ML, Schmitz AJ, Thole JM, Bonner HK, Otegui MS, Nielsen E (2006) A role for the RabA4b effector protein PI-4Kbeta1 in polarized expansion of root hair cells in Arabidopsis thaliana. J Cell Biol 172:991–998CrossRefPubMedGoogle Scholar
  48. 48.
    Preuss ML, Serna J, Falbel TG, Bednarek SY, Nielsen E (2004) The Arabidopsis Rab GTPase RabA4b localizes to the tips of growing root hair cells. Plant Cell 16:1589–1603CrossRefPubMedGoogle Scholar
  49. 49.
    Ramachandran S, Christensen HE, Ishimaru Y, Dong CH, Chao-Ming W, Cleary AL, Chua NH (2000) Profilin plays a role in cell elongation, cell shape maintenance, and flowering in Arabidopsis. Plant Physiol 124:1637–1647CrossRefPubMedGoogle Scholar
  50. 50.
    Reisen D, Hanson MR (2007) Association of six YFP-myosin XI-tail fusions with mobile plant cell organelles. BMC Plant Biol 7:6CrossRefPubMedGoogle Scholar
  51. 51.
    Ringli C, Baumberger N, Diet A, Frey B, Keller B (2002) ACTIN2 is essential for bulge site selection and tip growth during root hair development of Arabidopsis. Plant Physiol 129:1464–1472CrossRefPubMedGoogle Scholar
  52. 52.
    Sagi M, Fluhr R (2001) Superoxide production by plant homologues of the gp91(phox) NADPH oxidase. Modulation of activity by calcium and by tobacco mosaic virus infection. Plant Physiol 126:1281–1290CrossRefPubMedGoogle Scholar
  53. 53.
    Sakai T, Honing H, Nishioka M, Uehara Y, Takahashi M, Fujisawa N, Saji K, Seki M, Shinozaki K, Jones MA, Smirnoff N, Okada K, Wasteneys GO (2008) Armadillo repeat-containing kinesins and a NIMA-related kinase are required for epidermal-cell morphogenesis in Arabidopsis. Plant J 53:157–171CrossRefPubMedGoogle Scholar
  54. 54.
    Schiefelbein J, Galway M, Masucci J, Ford S (1993) Pollen tube and root-hair tip growth is disrupted in a mutant of Arabidopsis thaliana. Plant Physiol 103:979–985CrossRefPubMedGoogle Scholar
  55. 55.
    Schiefelbein JW, Somerville C (1990) Genetic control of root hair development in Arabidopsis thaliana. Plant Cell 2:235–243CrossRefPubMedGoogle Scholar
  56. 56.
    Sheahan MB, Staiger CJ, Rose RJ, McCurdy DW (2004) A green fluorescent protein fusion to actin-binding domain 2 of Arabidopsis fimbrin highlights new features of a dynamic actin cytoskeleton in live plant cells. Plant Physiol 136:3968–3978CrossRefPubMedGoogle Scholar
  57. 57.
    Sieberer BJ, Timmers AC, Lhuissier FG, Emons AM (2002) Endoplasmic microtubules configure the subapical cytoplasm and are required for fast growth of Medicago truncatula root hairs. Plant Physiol 130:977–988CrossRefPubMedGoogle Scholar
  58. 58.
    Smith, L.G., and D.G. Oppenheimer (2005) Spatial control of cell expansion by the plant cytoskeleton. Annu Rev Cell Dev Biol. 21:271–295Google Scholar
  59. 59.
    Sparkes IA, Teanby NA, Hawes C (2008) Truncated myosin XI tail fusions inhibit peroxisome, Golgi, and mitochondrial movement in tobacco leaf epidermal cells: a genetic tool for the next generation. J Exp Bot 59:2499–2512CrossRefPubMedGoogle Scholar
  60. 60.
    Swarup R, Friml J, Marchant A, Ljung K, Sandberg G, Palme K, Bennett M (2001) Localization of the auxin permease AUX1 suggests two functionally distinct hormone transport pathways operate in the Arabidopsis root apex. Genes Dev 15:2648–2653CrossRefPubMedGoogle Scholar
  61. 61.
    Takahashi H, Hirota K, Kawahara A, Hayakawa E, Inoue Y (2003) Randomization of cortical microtubules in root epidermal cells induces root hair initiation in lettuce (Lactuca sativa L.) seedlings. Plant Cell Physiol 44:350–359CrossRefPubMedGoogle Scholar
  62. 62.
    Takeda S, Gapper C, Kaya H, Bell E, Kuchitsu K, Dolan L (2008) Local positive feedback regulation determines cell shape in root hair cells. Science 319:1241–1244CrossRefPubMedGoogle Scholar
  63. 63.
    Tang XJ, Hepler PK, Scordilis SP (1989) Immunochemical and immunocytochemical identification of a myosin heavy chain polypeptide in Nicotiana pollen tubes. J Cell Sci 92(Pt 4):569–574PubMedGoogle Scholar
  64. 64.
    Thole JM, Vermeer JE, Zhang Y, Gadella TW Jr, Nielsen E (2008) Root hair defective4 encodes a phosphatidylinositol-4-phosphate phosphatase required for proper root hair development in Arabidopsis thaliana. Plant Cell 20:381–395CrossRefPubMedGoogle Scholar
  65. 65.
    Timmers AC, Vallotton P, Heym C, Menzel D (2007) Microtubule dynamics in root hairs of Medicago truncatula. Eur J Cell Biol 86:69–83CrossRefPubMedGoogle Scholar
  66. 66.
    Tominaga M, Morita K, Sonobe S, Yokota E, Shimmen T (1997) Microtubules regulate the organization of actin filaments at the cortical region in root hair cells of hydrocharis. Protoplasma 199:83–92CrossRefGoogle Scholar
  67. 67.
    Tominaga M, Yokota E, Sonobe S, Shimmen T (2000) Mechanism of inhibition of cytoplasmic streaming by a myosin inhibitor, 2, 3-butanedione monoxime. Protoplasma 213:46–54CrossRefGoogle Scholar
  68. 68.
    Traas JA, Braat P, Emons AM, Meekes H, Derksen J (1985) Microtubules in root hairs. J Cell Sci 76:303–320PubMedGoogle Scholar
  69. 69.
    Van Bruaene N, Joss G, Van Oostveldt P (2004) Reorganization and in vivo dynamics of microtubules during Arabidopsis root hair development. Plant Physiol 136:3905–3919CrossRefPubMedGoogle Scholar
  70. 70.
    Very AA, Davies JM (2000) Hyperpolarization-activated calcium channels at the tip of Arabidopsis root hairs. Proc Natl Acad Sci USA 97:9801–9806CrossRefPubMedGoogle Scholar
  71. 71.
    Voigt B, Timmers AC, Samaj J, Muller J, Baluska F, Menzel D (2005) GFP-FABD2 fusion construct allows in vivo visualization of the dynamic actin cytoskeleton in all cells of Arabidopsis seedlings. Eur J Cell Biol 84:595–608CrossRefPubMedGoogle Scholar
  72. 72.
    Wang YS, Yoo CM, Blancaflor EB (2008) Improved imaging of actin filaments in transgenic Arabidopsis plants expressing a green fluorescent protein fusion to the C- and N-termini of the fimbrin actin-binding domain 2. New Phytol 177:525–536PubMedGoogle Scholar
  73. 73.
    Whittington AT, Vugrek O, Wei KJ, Hasenbein NG, Sugimoto K, Rashbrooke MC, Wasteneys GO (2001) MOR1 is essential for organizing cortical microtubules in plants. Nature 411:610–613CrossRefPubMedGoogle Scholar
  74. 74.
    Wymer CL, Bibikova TN, Gilroy S (1997) Cytoplasmic free calcium distributions during the development of root hairs of Arabidopsis thaliana. Plant J 12:427–439CrossRefPubMedGoogle Scholar
  75. 75.
    Xue HW, Chen X, Mei Y (2009) Function and regulation of phospholipid signalling in plants. Biochem J 421:145–156CrossRefPubMedGoogle Scholar
  76. 76.
    Yalovsky S, Bloch D, Sorek N, Kost B (2008) Regulation of membrane trafficking, cytoskeleton dynamics, and cell polarity by ROP/RAC GTPases. Plant Physiol 147:1527–1543CrossRefPubMedGoogle Scholar
  77. 77.
    Yang G, Gao P, Zhang H, Huang S, Zheng ZL (2007) A mutation in MRH2 kinesin enhances the root hair tip growth defect caused by constitutively activated ROP2 small GTPase in Arabidopsis. PLoS ONE 2:e1074CrossRefPubMedGoogle Scholar
  78. 78.
    Yokota E, Muto S, Shimmen T (2000) Calcium-calmodulin suppresses the filamentous actin-binding activity of a 135-kilodalton actin-bundling protein isolated from lily pollen tubes. Plant Physiol 123:645–654CrossRefPubMedGoogle Scholar
  79. 79.
    Yoo CM, Wen J, Motes CM, Sparks JA, Blancaflor EB (2008) A class I ADP-ribosylation factor GTPase-activating protein is critical for maintaining directional root hair growth in Arabidopsis. Plant Physiol 147:1659–1674CrossRefPubMedGoogle Scholar
  80. 80.
    Zheng M, Beck M, Muller J, Chen T, Wang X, Wang F, Wang Q, Wang Y, Baluska F, Logan DC, Samaj J, Lin J (2009) Actin turnover is required for myosin-dependent mitochondrial movements in Arabidopsis root hairs. PLoS ONE 4:e5961CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  1. 1.Department of Biochemistry and Cellular and Molecular BiologyUniversity of TennesseeKnoxvilleUSA

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