Skip to main content
SpringerLink
Log in

Calcium in Root Hair Growth

  • Chapter
  • First Online:
Plant Cell Monographs

Part of the book series: Plant Cell Monographs

  • 11 Accesses

Abstract

The growth of cells as diverse as fungal hyphae, pollen tubes, algal rhizoids, and root hairs is characterized by a highly localized control of cell expansion confined to the growing tip. The cellular regulators that have been shown to maintain this spatial localization of growth range from monomeric G-proteins and the actin cytoskeleton to protein kinases and phospholipid-modulating enzymes. A central theme in the proposed mode of action of most of these factors is either regulation of, or response to, the concentration of cytoplasmic Ca2+. For example, a tip-focused Ca2+gradient is associated with the growing point of the root hair and is thought to mediate spatial control of membrane trafficking and the cytoskeleton. Key advances in our understanding of how Ca2+acts in this system have been the recent identification of some of the Ca2+channels and transporters likely responsible for modulating this Ca2+gradient and the likely central role for reactive oxygen species (ROS) in regulating these events. Similarly, molecular identification of Ca2+-responsive elements, such as Ca2+-dependent protein kinases, likely to interact with the tip-focused gradient has begun. This Ca2+-signaling system appears to interact with many of the other components of the tip growth system, including monomeric G-proteins, phospholipases, and the cytoskeleton, helping integrate these activities to facilitate the localization of growth.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution

Institutional subscriptions

References

  • Alattia JR, Ames JB, Porumb T, Tong KI, Heng YM, Ottensmeyer P, Kay CM, Ikura M (1997) Lateral self-assembly of E-cadherin directed by cooperative calcium binding. FEBS Lett 417:405–408

    Article  PubMed  CAS  Google Scholar 

  • Allwood EG, Anthony RG, Smertenko AP, Reichelt S, Drobak BK, Doonan JH, Weeds AG, Hussey PJ (2002) Regulation of the pollen-specific actin-depolymerizing factor LlADF1. Plant Cell 14:2915–2927

    Article  PubMed  CAS  Google Scholar 

  • Allwood EG, Smertenko AP, Hussey PJ (2001) Phosphorylation of plant actin depolymerising factor by calmodulin-like domain protein kinase. FEBS Lett 499:97–100

    Article  PubMed  CAS  Google Scholar 

  • Bankaitis VA, Aitken JR, Cleves AE, Dowhan W (1990) An essential role for a phospholipid transfer protein in yeast Golgi function. Nature 347:561–562

    Article  PubMed  ADS  CAS  Google Scholar 

  • Battey NH, James NC, Greenland AJ, Brownlee C (1999) Exocytosis and endocytosis. Plant Cell 11:643–659

    Article  PubMed  CAS  Google Scholar 

  • Bibikova TN, Blancaflor EB, Gilroy S (1999) Microtubules regulate tip growth and orientation in root hairs of Arabidopsis thaliana. Plant J 17:657–665

    Article  PubMed  CAS  Google Scholar 

  • Bibikova TN, Gilroy S (2000) Calcium in root hair growth and development. In: Ridge R, Emons AM, (eds) The cellular and molecular biology of root hairs. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Bibikova TN, Gilroy S (2002) Root hair development. J Plant Growth Regul 21:383–415

    Article  CAS  Google Scholar 

  • Bibikova TN, Zhigilei A, Gilroy S (1997) Root hair growth in Arabidopsis thalianais directed by calcium and an endogenous polarity. Planta 203:495–505

    Article  PubMed  CAS  Google Scholar 

  • Blackbourn HD, Barker PJ, Huskisson NS, Battey NH (1992) Properties and partial protein-sequence of plant annexins. Plant Physiol 99:864–871

    PubMed  CAS  Google Scholar 

  • Blanchoin L, Pollard TD (1999) Mechanism of interaction of Acanthamoeba actophorin(ADF/cofilin) with actin filaments. J Biol Chem 274:15538–15546

    Article  PubMed  CAS  Google Scholar 

  • Blancaflor EB, Gilroy S (2000) Plant cell biology in the new millennium: new tools and new insights. Am J Bot 87:1547–1560

    Article  PubMed  CAS  Google Scholar 

  • Brownlee C, Bouget FY (1998) Polarity determination in Fucus: from zygote to multicellular embryo. Semin Cell Dev Biol 9:179–185

    Article  PubMed  CAS  Google Scholar 

  • Brownlee C, Goddard H, Hetherington AM, Peake L (1999) Specificity and integration of responses: Ca2+as a signal in polarity and osmotic regulation. J Exp Bot 50:1001–1011

    Article  CAS  Google Scholar 

  • Burgoyne RD, Clague MJ (2003) Calcium and calmodulin in membrane fusion. Biochim Biophys Acta 1641:137–143

    Article  PubMed  CAS  Google Scholar 

  • Calvert CM, Gant SJ, Bowles DJ (1996) Tomato annexins p34 and p35 bind to F-actin and exhibit nucleotide phosphodiesterase activity inhibited by phospholipid binding. Plant Cell 8:333–342

    Article  PubMed  CAS  Google Scholar 

  • Campanoni P, Blatt MR (2007) Membrane trafficking and polar growth in root hairs and pollen tubes. J Exp Bot 58(1):65–74

    PubMed  CAS  Google Scholar 

  • Carlier MF, Laurent V, Santolini J, Melki R, Didry D, Xia GX, Hong Y, Chua NH, Pantaloni D (1997) Actin depolymerizing factor (ADF/cofilin) enhances the rate of filament turnover: implication in actin-based motility. J Cell Biol 136:1307–1322

    Article  PubMed  CAS  Google Scholar 

  • Carol RJ, Dolan L (2002) Building a hair: tip growth in Arabidopsis thalianaroot hairs. Phil Trans R Soc Lond B 357:815–821

    Article  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 s patially regulates growth in root hair cells. Nature 438:1013–1016

    Article  PubMed  ADS  CAS  Google Scholar 

  • Carroll AD, Moyen C, Van Kesteren P, Tooke F, Battey NH, Brownlee C (1998) Ca2+, annexins, and GTP modulate exocytosis from maize root cap protoplasts. Plant Cell 10:1267–1276

    Article  PubMed  CAS  Google Scholar 

  • Choe CU, Ehrlich BE (2006) The inositol 1,4,5-trisphosphate receptor (IP3R) and its regulators: sometimes good and sometimes bad teamwork. Sci STKE 363:15

    Google Scholar 

  • Clark GB, Dauwalder M, Roux SJ (1992) Purification and immunolocalization of an annexin-like protein in pea-seedlings. Planta 187:1–9

    Article  PubMed  CAS  Google Scholar 

  • Clark GB, Roux SJ (1995) Annexins of plant cells. Plant Physiol 109:1133–1139

    Article  PubMed  CAS  Google Scholar 

  • Clarkson DT, Brownlee C, Ayling SM (1988) Cytoplasmic calcium measurements in intact higher plant cells results from fluorescence ratio imaging of fura-2. J Cell Sci 91:71–80

    CAS  Google Scholar 

  • Coelho SM, Taylor AR, Ryan KP, Sousa-Pinto I, Brown MT, Brownlee C (2002) Spatiotemporal patterning of reactive oxygen production and Ca2+wave propagation in Fucus rhizoid cells. Plant Cell 14:2369–2381

    Article  PubMed  CAS  Google Scholar 

  • Cyr RJ (1994) Microtubules in plant morphogenesis - role of the cortical array. Annu Rev Cell Biol 10:153–180

    Article  PubMed  CAS  Google Scholar 

  • Delmer DP, Potikha TS (1997) Structures and functions of annexins in plants. Cell Mol Life Sci 53:546–553

    Article  PubMed  CAS  Google Scholar 

  • Demkiv OT, Khorkavtsiv YD, Kardash AR (1994) Intracellular pH during growth and differentiation of the gametophyte Funaria hygrometricacells. Russ J Plant Physiol 41:84–87

    Google Scholar 

  • Derksen J (1996) Pollen tubes: a model system for plant cell growth. Bot Acta 109:341–345

    CAS  Google Scholar 

  • Dixit R, Cyr R, Gilroy S (2006) Using intrinsically fluorescent proteins for plant cell imaging. Plant J 45:599–615

    Article  PubMed  CAS  Google Scholar 

  • Dolan L, Duckett CM, Grierson C, Linstead P, Schneider K, Lawson E, Dean C, Poethig S, Roberts K (1994) Clonal relationships and cell patterning in the root epidermis of Arabidopsis. Development 120:2465–2474

    CAS  Google Scholar 

  • Dong CH, Xia GX, Honga Y, Ramachandrana S, Kosta B, Chua NH (2001) ADF proteins are involved in the control of flowering and regulate F-actin organization, cell expansion, and organ growth in Arabidopsis. Plant Cell 13:1333–1346

    Article  PubMed  CAS  Google Scholar 

  • Dowd PE, Coursol S, Skirpan AL, Kao TH, Gilroy S (2006) Petunia Phospholipase C is involved in pollen tube growth. Plant Cell 18:1438–1453

    Article  PubMed  CAS  Google Scholar 

  • Drubin DG, Nelson WJ (1996) Origins of cell polarity. Cell 84:335–344

    Article  PubMed  CAS  Google Scholar 

  • Dutta R, Robinson KR (2004) Identification and characterization of stretch-activated ion channels in pollen protoplasts. Plant Physiol 135:1398–1406

    Article  PubMed  CAS  Google Scholar 

  • Emons AMC (1987) The cytoskeleton and secretory vesicles in root hairs of Equisetum and Limnobium and cytoplasmic streaming in root hairs of Equisetum. Ann Bot 60:625–632

    Google Scholar 

  • Ehrhardt DW, Wais R, Long SR (1996) Calcium spiking in plant root hairs responding to Rhizobium nodulation signals. Cell 85:673–681

    Article  PubMed  CAS  Google Scholar 

  • Esseling JJ, Lhuissier FG, Emons AM (2003) Nod factor-induced root hair curling: continuous polar growth towards the point of nod factor application. Plant Physiol 132:1982–1988

    Article  PubMed  CAS  Google Scholar 

  • Fan X, Hou J, Chen X, Chaudhry F, Staiger CJ, Ren H (2004) Identification and characterization of a Ca2+- dependent actin-filament severing protein from lily pollen. Plant Physiol 136:3979–3989

    Article  PubMed  CAS  Google Scholar 

  • Feijo JA, Sainhas J, Holdaway-Clarke T, Cordeiro MS, Kunkel JG, Hepler PK (2001) Cellular oscillations and the regulation of growth: the pollen tube paradigm. Bioessays 23:86–94

    Article  PubMed  CAS  Google Scholar 

  • Felle HH, Hepler PK (1997) The cytosolic Ca2+concentration gradient of Sinapis albaroot hairs as revealed by Ca2+- selective microelectrode tests and Fura-Dextran ratio imaging. Plant Physiol 114:39–45

    PubMed  CAS  Google Scholar 

  • Felle HH, Kondorosi E, Kondorosi A, Schultze M (1999) Nod factors modulate the concentration of cytosolic free calcium differently in growing and non-growing root hairs of Medicago sativaL. Planta 209:207–212

    Article  PubMed  CAS  Google Scholar 

  • Fisher DD, Gilroy S, Cyr RJ (1996) Evidence for opposing effects of calmodulin on cortical microtubules. Plant Phys 112:1079–1087

    CAS  Google Scholar 

  • Foreman J, Demidchik V, Bothwell JHF, 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 422:442–446

    Article  PubMed  ADS  CAS  Google Scholar 

  • Franklin-Tong VE, Drøbak BK, Allan AC, Watkins PAC, Trewavas AJ (1996) Growth of pollen tubes of Papaver rhoeasis regulated by a slow moving calcium wave propagated by inositol triphosphate. Plant Cell 8:1305–1321

    Article  PubMed  CAS  Google Scholar 

  • Fricker MD, Blancaflor EB, Meyer A, Parsons A, Plieth C, Tlaka M, Gilroy S (2001) Fluorescent probes for living cells. In: C Hawes and B Satiat-Jeunemaitre (eds) Cell Biology, A Practical Approach. Oxford University Press, Oxford, pp 35–85

    Google Scholar 

  • 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 152:1019–1032

    Article  PubMed  CAS  Google Scholar 

  • Galway ME, Heckman JW, Schiefelbein JW (1997) Growth and ultrastructure of Arabidopsisroot hairs: the rhd3mutation alters vacuole enlargement and tip growth. Planta 201:209–218

    Article  PubMed  CAS  Google Scholar 

  • Garril A, Jackson SL, Lew RR, Heath IB (1993) Ion channel activity and tip growth – tip-localized stretch-activated channels generate an essential Ca2+gradient in the oomycete Saprolegnia Ferax. Eur J Cell Biol 60:358–365

    Google Scholar 

  • Gerke V, Moss SE (2002) Annexins: From structure to function. Physiol Rev 82:331–371

    PubMed  CAS  Google Scholar 

  • Gilroy S, Jones DL (2000) Through form to function: root hair development and nutrient uptake. Trends Plant Sci 5:56–60

    Article  PubMed  CAS  Google Scholar 

  • Gilroy S (1997) Fluorescence microscopy of living plant cells. Annu Rev Plant Physiol Plant Mol Biol 48:165–190

    Article  PubMed  CAS  Google Scholar 

  • Gruenberg J, Emans N (1993) Annexins in membrane traffic. Trends Cell Biol 3:224–227

    Article  PubMed  CAS  Google Scholar 

  • Gu Y, Fu Y, Dowd P, Li S, Vernoud V, Gilroy S, Yang Z (2005) A Rho family GTPase controls actin dynamics and tip growth via two counteracting downstream pathways in pollen tubes. J Cell Biol 169:127–138

    Article  PubMed  CAS  Google Scholar 

  • Gungabissoon RA, Jiang CJ, Drobak BK (1998) Interaction of maize actin depolymerising factor with actin and phosphoinositides and its inhibition of plant phospholipase C. Plant J 16:689–696

    Article  CAS  Google Scholar 

  • Hahm SH, Saunders MJ (1991) Cytokinin increases intracellular calcium in Funaria: detection with Indo-1. Cell Calcium 12:675–681

    Article  PubMed  CAS  Google Scholar 

  • Hausser I, Herth W, Reiss HD (1984) Calmodulin in tip-growing plant cells visualized by fluorescing calmodulin-binding phenothiazines. Planta 162:33–39

    Article  CAS  Google Scholar 

  • Helling D, Possart A, Cottier S, Klahre U, Kost B (2006) Pollen tube tip growth depends on plasma membrane polarization mediated by tobacco PLC3 activity and endocytic membrane recycling. Plant Cell 18:3519–3534

    Article  PubMed  CAS  Google Scholar 

  • Hepler PK, Waayne RO (1985) Calcium and plant development. Annu Rev Plant Physiol 36:397–439

    Article  CAS  Google Scholar 

  • Herrmann A, Felle HH (1995) Tip growth in root hair-cells of Sinapis-albaL - significance of internal and external Ca2+and pH. New Phytol 129:523–533

    Article  CAS  Google Scholar 

  • Hetherington AM, Brownlee C (2004) The generation of Ca2+signals in plants. Annu Rev Plant Biol 55:401–427

    Article  PubMed  CAS  Google Scholar 

  • Holdaway-Clarke TL, Feijo JA, Hackett GR, Kunkel JG, Hepler PK (1997) Pollen tube growth and the intracellular cytosolic calcium gradient oscillate in phase while extracellular calcium influx is delayed. Plant Cell 9:1999–2010

    Article  PubMed  CAS  Google Scholar 

  • Holdaway-Clarke TL, Hepler PK (2003) Control of pollen tube growth: role of ion gradients and fluxes. New Phytol 159:539–563

    Article  CAS  Google Scholar 

  • Holzinger A, Callaham OA, Hepler PK, Meindl U (1995) Free calcium in Mirasterias– local gradients are not detected in growing lobes. Eur J Cell Biol 67:363–371

    PubMed  CAS  Google Scholar 

  • Homann U, Tester M (1997) Ca2+- independent and Ca2+/GTP-binding protein-controlled exocytosis in a plant cell. Proc Natl Acad Sci USA 94:6565–6570

    Article  PubMed  ADS  CAS  Google Scholar 

  • Huang S, Robinson RC, Gao LY, Matsumoto T, Brunet A, Blanchoin L, Staiger CJ (2005) ArabidopsisVILLIN1 generates actin filament cables that are resistant to depolymerization. Plant Cell 17:486–501

    Article  PubMed  CAS  Google Scholar 

  • Hurst SR, Kropf DL (1991) Ionic requirements for establishment of an embryonic axis in Pelvetiazygotes. Planta 185:27–33

    Article  CAS  Google Scholar 

  • Hyde GJ, Heath JB (1995) Ca2+-dependent polarization axis establishment in the tip- growing organism, Saprolegnia-ferax, by gradients of the ionophore A23187. Eur J Cell Biol 67:356–362

    PubMed  CAS  Google Scholar 

  • Ikebuchi NW, Wiseman DM (1990) Calcium-dependent regulation of actin filament bundling by lipocortin-85. J Biol Chem 265:3392–342

    PubMed  CAS  Google Scholar 

  • Ivashuta S, Liu JY, Liu JQ, Lohar DP, Haridas S, Bucciarelli B, VandenBosch KA, Vance CP, Harrison MJ, Gantt JS (2005) RNA interference identifies a calcium-dependent protein kinase involved in Medicago truncatularoot development. Plant Cell 17:2911–2921

    Article  PubMed  CAS  Google Scholar 

  • Jiang L, Yang SL, Xie LF, Puah CS, Zhang XQ, Yang WC, Sundaresan V, Ye D (2005) VANGUARD1 encodes a pectin methylesterase that enhances pollen tube growth in the Arabidopsisstyle and transmitting tract. Plant Cell 17:584–596

    Article  PubMed  CAS  Google Scholar 

  • Jones DL, Gilroy S, Larsen PB, Howell SH, Kochian LV (1998) Effect of aluminum on cytoplasmic Ca2+homeostasis in root hairs of Arabidopsis thaliana(L.). Planta 206:378–387

    Article  PubMed  CAS  Google Scholar 

  • Jones DL, Shaff JE, Kochian LV (1995) Role of calcium and other ions in directing root hair tip growth in Limnobium stoloniferum: I. Inhibition of tip growth by aluminum. Planta 197:672–680

    Article  CAS  Google Scholar 

  • Kanamori N, Madsen LH, Radutoiu S, Frantescu M, Quistgaard EM, Miwa H, Downie JA, James EK, Felle HH, Haaning LL, Jensen TH, Sato S, Nakamura Y, Tabata S, Sandal N, Stougaard J (2006) A nucleoporin is required for induction of Ca2+ spiking in legume nodule development and essential for rhizobial and fungal symbiosis. Proc Natl Acad Sci USA 103:359–364

    Article  PubMed  ADS  CAS  Google Scholar 

  • Ketelaar T, de Ruijter NC, Emons AM (2003) Unstable F-actin specifies the area and microtubule direction of cell expansion in Arabidopsisroot hairs. Plant Cell 15:285–292

    Article  PubMed  CAS  Google Scholar 

  • Kinoshita T, Nishimura M, Shimazaki K (1995) Cytosolic concentration of Ca2+regulates the plasma membrane H+-ATPase in guard cells of Fava bean. Plant Cell 7:1333–1342

    Article  PubMed  CAS  Google Scholar 

  • Klusener B, Boheim G, Liss H, Engelberth J, Weiler EW (1995) Gadolinium-sensitive, voltage-dependent calcium-release channels in the endoplasmic-reticulum of a higher-plant mechanoreceptor organ. EMBO J 14:2708–2714

    PubMed  CAS  Google Scholar 

  • Kohno T, Shimmen T (1987) Ca2+induced fragmentation of actin-filaments in pollen tubes. Protoplasma 141:177–179

    Article  CAS  Google Scholar 

  • Kost B, Lemichez E, Spielhofer P, Hong Y, Tolias K, Carpenter C, Chua NH (1999) Rac homologues and compartmentalized phosphatidylinositol 4, 5-bisphosphate act in a common pathway to regulate polar pollen tube growth. J Cell Biol 145:317–330

    Article  PubMed  CAS  Google Scholar 

  • Lancelle SA, Hepler PK (1992) Ultrastructure of freeze substituted pollen tubes of Lilium longiflorum. Protoplasma 167:215–230

    Article  Google Scholar 

  • Lee S, Lee EJ, Yang EJ, Lee JE, Park AR, Song WH, Park OK (2004) Proteomic identification of annexins, calcium-dependent membrane binding proteins that mediate osmotic stress and abscisic acid signal transduction in Arabidopsis. Plant Cell 16:1378–1391

    Article  PubMed  CAS  Google Scholar 

  • Li L, Kim BG, Cheong YH, Pandey GK, Luan S (2006a) A Ca2+signaling pathway regulates a K+channel for low-K response in Arabidopsis. Proc Natl Acad Sci USA 103:12625–12630

    Article  ADS  CAS  Google Scholar 

  • Li M, Qin C, Welti R, Wang X (2006b) Double knockouts of phospholipases Dzeta1 and Dzeta2 in Arabidopsisaffect root elongation during phosphate-limited growth but do not affect root hair patterning. Plant Physiol 140:761–770

    Article  CAS  Google Scholar 

  • Li H, Lin YK, 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 11:1731–1742

    Article  PubMed  CAS  Google Scholar 

  • Lin YK, Yang ZB (1997) Inhibition of pollen tube elongation by microinjected anti-Rop1Ps antibodies suggests a crucial role for Rho-type GTPases in the control of tip growth. Plant Cell 9:1647–1659

    Article  PubMed  CAS  Google Scholar 

  • Love J, Brownlee C, Trewavas AJ (1997) Ca2+and calmodulin dynamics during photopolarization in Fucus serratuszygotes. Plant Physiol 115:249–261

    PubMed  CAS  Google Scholar 

  • Malho R (1998) Expanding tip-growth theory. Trends Plant Sci 3:40–43

    Google Scholar 

  • Malho R, Trewavas AJ (1996) Localized apical increases of cytosolic free calcium control pollen tube orientation. Plant Cell 8:1935–1949

    Article  PubMed  CAS  Google Scholar 

  • Messerli MA, Creton R, Jaffe LF, Robinson KR (2000) Periodic increases in elongation precede increases in cytosolic Ca2+during pollen tube growth. Dev Biol 222:84–98

    Article  PubMed  CAS  Google Scholar 

  • Messerli MA, Danuser G, Robinson KP (1999) Pulsatile influxes of H+, K+and Ca2+tag growth pulses of Lilium longiflorumpollen tubes. J Cell Sci 112:1497–1509

    PubMed  CAS  Google Scholar 

  • Messerli M, Robinson KR (1997) Tip localized Ca2+pulses are coincident with peak pulsatile growth rates in pollen tubes of Lilium longiflorum. J Cell Sci 110:1269–1278

    PubMed  CAS  Google Scholar 

  • Miller DD, Callaham DA, Gross DJ, Hepler PK (1992) Free Ca2+gradient in growing pollen tubes of Lilium longiflorum. J Cell Sci 101:7–12

    CAS  Google Scholar 

  • Miller DD, Leferink-ten Klooster HB, Emons AMC (2000) Lipochito-oligosaccharide nodulation factors stimulate cytoplasmic polarity with longitudinal endoplasmic reticulum and vesicles at the tip in vetch root hairs. Mol Plant Microbe Interact 13:1385–1390

    Article  PubMed  CAS  Google Scholar 

  • 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 17:141–154

    Article  CAS  Google Scholar 

  • Miwa H, Sun J, Oldroyd GE, Downie JA (2006) Analysis of Nod-factor-induced calcium signaling in root hairs of symbiotically defective mutants of Lotus japonicus. Mol Plant Microbe Interact 19:914–923

    Article  PubMed  CAS  Google Scholar 

  • Miyawaki A, Llopis J, Heim R, McCaffery JM, Adams JA, Ikura M, Tsien RY (1997) Fluorescent indicators for Ca2+based on green fluorescent proteins and calmodulin. Nature 388:882–887

    Article  PubMed  ADS  CAS  Google Scholar 

  • Molendijk AJ, Bischoff F, Rajendrakumar CS, Friml J, Braun M, Gilroy S, Palme K (2001) Arabidopsis thalianaRop GTPases are localized to tips of root hairs and control polar growth. EMBO J 20:2779–2788

    Article  PubMed  CAS  Google Scholar 

  • Monteiro D, Liu QL, Lisboa S, Scherer GEF, Quader H, Malho R (2005) Phosphoinositides and phosphatidic acid regulate pollen tube growth and reorientation through modulation of [Ca2+]cand membrane secretion. J Exp Bot 56:1665–1674

    Article  PubMed  CAS  Google Scholar 

  • Moutinho A, Trewavas AJ, Malho R (1998) Relocation of a Ca2+- dependent protein kinase activity during pollen tube reorientation. Plant Cell 10:1499–1509

    Article  PubMed  CAS  Google Scholar 

  • Muir SR, Sanders D (1997) Inositol 1,4,5-trisphosphate-sensitive Ca2+release across nonvacuolar membranes in cauliflower. Plant Phys 114:1511–1521

    Article  CAS  Google Scholar 

  • Nagai T, Yamada S, Tominaga T, Ichikawa M, Miyawaki A (2004) Expanded dynamic range of fluorescent indicators for Ca(2+) by circularly permuted yellow fluorescent proteins. Proc Natl Acad Sci USA 101:10554–10559

    Article  PubMed  ADS  CAS  Google Scholar 

  • Ohashi Y, Oka A, Rodrigues-Pousada R, Possenti M, Ruberti I, Morelli G, Aoyama T (2003) Modulation of phospholipid signaling by GLABRA2 in root-hair pattern formation. Science 300:1427–1430

    Article  PubMed  ADS  CAS  Google Scholar 

  • Oheim M, Kirchhoff F, Stuhmer W (2006) Calcium microdomains in regulated exocytosis. Cell Calcium 40:423–439

    Article  PubMed  CAS  Google Scholar 

  • Parton RM, Fischer-Parton S, Watahiki MK, Trewavas AJ (2001) Dynamics of the apical vesicle accumulation and the rate of growth are related in individual pollen tubes. J Cell Sci 114:2685–2695

    PubMed  CAS  Google Scholar 

  • Peiter E, Maathuis FJ, Mills LN, Knight H, Pelloux J, Hetherington AM, Sanders D (2005) The vacuolar Ca2+-activated channel TPC1 regulates germination and stomatal movement. Nature 434(7031):404–408

    Article  PubMed  ADS  CAS  Google Scholar 

  • Picton JM, Steer MW (1983) Evidence for the role of Ca2+ions in tip extension in pollen tubes. Protoplasma 115:1–17

    Article  Google Scholar 

  • Preuss ML, Schmitz AJ, Thole JM, Bonner HK, Otegui MS, Nielsen E (2006) A role for the RabA4b effector protein PI-4Kβ1in polarized expansion of root hair cells in Arabidopsis thaliana. J Cell Biol 172:991–998

    Article  PubMed  CAS  Google Scholar 

  • Preuss ML, Serna J, Falbel TG, Bednarek SY, Nielsen E (2004) The ArabidopsisRab GTPase RabA4b localizes to the tips of growing root hair cells. Plant Cell 16(6):1589–603

    Article  PubMed  CAS  Google Scholar 

  • Pu R, Robinson KR (1998) Cytoplasmic calcium gradients and calmodulin in the early development of the fucoid alga Pelvetia compressa. J Cell Sci 111:3197–3207

    PubMed  CAS  Google Scholar 

  • Rato C, Monteiro D, Hepler PK, Malho R (2004) Calmodulin activity and cAMP signalling modulate growth and apical secretion in pollen tubes. Plant J 38:887–897

    Article  PubMed  CAS  Google Scholar 

  • Reintanz B, Szyroki A, Ivashikina N, Ache P, Godde M, Becker D, Palme K, Hedrich R (2002) AtKC1, a silent Arabidopsispotassium channel alpha -subunit modulates root hair K+influx. Proc Natl Acad Sci USA 99:4079–4084

    Article  PubMed  ADS  CAS  Google Scholar 

  • Reissig JL, Kinney SG (1983) Calcium as a branching signal in Neurospora crassa. J Bacteriol 154:1397–1402

    PubMed  CAS  Google Scholar 

  • Robinson KR, Jaffe LF (1973) Ion movements in a developing fucoid egg. Dev Biol 35:349–361

    Article  PubMed  CAS  Google Scholar 

  • Rosen WG, Gawlik SR, Dashek WV, Siegesmund KA (1964) Fine structure and cytochemistry of Liliumpollen tubes. Am J Bot 51:61–71

    Article  CAS  Google Scholar 

  • de Ruijter NCA, Rook MB, Bisseling T, Emons AMC (1998) Lipochito-oligosaccharides re-initiate root hair tip growth in Vicia sativawith high calcium and spectrin-like antigen at the tip. Plant J 13:341–350

    Article  CAS  Google Scholar 

  • Schiefelbein JW, Shipley A, Rowse P (1992) Calcium influx at the tip of growing root-hair cells of Arabidopsis thaliana. Planta 187:455–459

    Article  CAS  Google Scholar 

  • Schiott M, Romanowsky SM, Baekgaard L, Jakobsen MK (2004) A plant plasma membrane Ca2+pump is required for normal pollen tube growth and fertilization. Proc Natl Acad Sci USA 101:9502–9507

    Article  PubMed  ADS  CAS  Google Scholar 

  • Schwab A, Finsterwalder F, Kersting U, Danker T, Oberleithner H (1997) Intracellular Ca2+distribution in migrating transformed epithelial cells. Pflugers Arch 434:70–76

    Article  PubMed  CAS  Google Scholar 

  • Shigaki T, Hirschi KD (2006) Diverse functions and molecular properties emerging for CAX cation/H+exchangers in plants. Plant Biol (Stuttg) 8:419–429

    Article  CAS  Google Scholar 

  • Sieberer BJ, Emons AMC (2003) Cytoarchitecture and pattern of cytoplasmic streaming in root hairs of Medicago truncatula during development and deformation by nodulation factors. Protoplasma 214:118–127

    Article  Google Scholar 

  • Sievers A, Schnepf E (1981) Morphogenesis and polarity in tubular cells with tip growth. In: Kiermayer O (ed) Cytomorphogenesis in Plants.Springer, Berlin Heidelberg New York, pp 265–299

    Google Scholar 

  • Shaw SL, Quatrano RS (1996) The role of targeted secretion in the establishment of cell polarity and the orientation of the division plane in Fucus zygotes. Development 122:2623–2630

    PubMed  CAS  Google Scholar 

  • Smertenko AP, Jiang CJ, Simmons NJ,Weeds AG, Davies DR, Hussey PJ (1998) Ser6 in the maize actin-depolymerizing factor, ZmADF3, is phosphorylated by a calcium stimulated protein kinase and is essential for the control of functional activity. Plant J 14:187–193

    Article  PubMed  CAS  Google Scholar 

  • Speksnijder JE, Miller AL, Weisenseel MH, Chen TH, Jaffe LF (1989) Calcium buffer injections block fucoid egg development by facilitating calcium diffusion. Proc Natl Acad Sci USA 86:6607–6661

    Article  PubMed  ADS  CAS  Google Scholar 

  • Sun J, Miwa H, Downie JA, Oldroyd GE (2007) Mastoparan activates calcium spiking analogous to Nod factor-induced responses in Medicago truncatula root hair cells. Plant Physiol 144:695–702

    Article  PubMed  CAS  Google Scholar 

  • Taylor AR, Manison NFH, Fernandez C, Wood J (1996) Spatial organization of calcium signaling involved in cell volume control in the Fucusrhizoid. Plant Cell 8:2015–2031

    Article  PubMed  CAS  Google Scholar 

  • Thiel G, Rupnik M, Zorec R (1994) Raising the cytosolic Ca2+concentration increases the membrane capacitance of maize coleoptile protoplasts: Evidence for Ca2+-stimulated exocytosis. Planta 195:305–308

    Article  CAS  Google Scholar 

  • Thion L, Mazars C, Nacry P, Bouchez D, Moreau M, Ranjeva R, Thuleau P (1998) Plasma membrane depolarization-activated calcium channels, stimulated by microtubule-depolymerizing drugs in wild-type Arabidopsis thalianaprotoplasts, display constitutively large activities and a longer half-life in ton 2 mutant cells affected in the organization of cortical microtubules. Plant J 13:603–610

    Article  PubMed  CAS  Google Scholar 

  • Tominaga M, Yokota E, Vidali L, Sonobe S, Hepler PK, Shimmen T (2000) The role of plant villin in the organization of the actin cytoskeleton, cytoplasmic streaming and the architecture of the transvacuolar strand in root hair cells of Hydrocharis. Planta 210:836–843

    Article  PubMed  CAS  Google Scholar 

  • Trewavas AJ, Malho R (1997) Signal perception and transduction: The origin of the phenotype. Plant Cell 9:1181–1195

    Article  PubMed  CAS  Google Scholar 

  • Very AA, Davies JM (2000) Hyperpolarization-activated calcium channels at the tip of Arabidopsisroot hairs. Proc Natl Acad Sci USA 97:9801–9806

    Article  PubMed  ADS  CAS  Google Scholar 

  • Vincent P, Chua M, Nogue F, Fairbrother A, Mekeel H, Xu Y, Allen N, Bibikova TN, Gilroy S, Bankaitis VA (2005) A Sec14p-nodulin domain phosphatidylinositol transfer protein polarizes membrane growth of Arabidopsis thalianaroot hairs. J Cell Biol 168:801–812

    Article  PubMed  CAS  Google Scholar 

  • Wang YF, Fan LM, Zhang WZ, Zhang W, Wu WH (2004) Ca2+-permeable channels in the plasma membrane of Arabidopsispollen are regulated by actin microfilaments. Plant Physiol 136:3892–3904

    Article  PubMed  CAS  Google Scholar 

  • Wang G, Lu L, Zhang CY, Singapuri A, Yuan S (2006) Calmodulin concentrates at the apex of growing hyphae and localizes to the Spitzenkorper in Aspergillus nidulans. Protoplasma 228:159–166

    Article  PubMed  CAS  Google Scholar 

  • Watson AJ, Barcroft LC (2001) Regulation of blastocyst formation. Front Biosci 6:D708–D730

    Article  PubMed  CAS  Google Scholar 

  • White PJ (1998) Calcium channels in the plasma membrane of root cells. Ann Bot 81:173–183

    Article  CAS  Google Scholar 

  • Wu G, Gu Y, Li S, Yang Z (2001) A genome-wide analysis of ArabidopsisRop-interactive CRIB motif-containing proteins that act as Rop GTPase targets. Plant Cell 13:2841–2856

    Article  PubMed  CAS  Google Scholar 

  • Wymer CL, Bibikova TN, Gilroy S (1997) Cytoplasmic free calcium distributions during the development of root hairs of Arabidopsis thaliana. Plant J 12:427–439

    Article  PubMed  CAS  Google Scholar 

  • Yokota E, Tominaga M, Mabuchi I, Tsuji Y, Staiger CJ, Oiwa K, Shimmen T (2005) Plant villin, lily P-135-ABP, possesses G-actin binding activity and accelerates the polymerization and depolymerization of actin in a Ca2+-sensitive manner. Plant Cell Physiol 46:1690–1703

    Article  PubMed  CAS  Google Scholar 

  • Yoon GM, Dowd PE, Gilroy S, McCubbin AG (2006) Calcium-dependent protein kinase isoforms in Petunia have distinct functions in pollen tube growth, including regulating polarity. Plant Cell 18:867–878

    Article  PubMed  CAS  Google Scholar 

  • Zielinski RE (1998) Calmodulin and calmodulin-binding proteins in plants. Annu Rev Plant Physiol Plant Mol Biol 49:697–725

    Article  PubMed  CAS  Google Scholar 

  • Zorec R, Tester M (1992) Cytoplasmic Ca2+stimulates exocytosis in a plant secretory cell. Biophys J 63:864–867

    Article  CAS  PubMed  Google Scholar 

  • Zorec R, Tester M (1993) Rapid pressure driven exocytosis–endocytosis cycle in a single plant cell. FEBS Lett 333:283–286

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank Drs. Gabriele Monshausen and Sarah Swanson for their critical reading of the manuscript. This work was supported by grants from the National Science Foundation.

Author information

Authors and Affiliations

  1. Department of Botany, University of Wisconsin, Birge Hall, 430 Lincoln Drive, Madison, USA

    T. Bibikova

Authors
  1. T. Bibikova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. Gilroy(✉)
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

Copyright information

© 2008 Springer-Verlag US

About this chapter

Cite this chapter

Bibikova, T., Gilroy(✉), S. (2008). Calcium in Root Hair Growth. In: Plant Cell Monographs. Springer, Berlin, Heidelberg. https://doi.org/10.1007/7089_2008_3

Download citation

  • DOI: https://doi.org/10.1007/7089_2008_3

  • Published:

  • Publisher Name: Springer, Berlin, Heidelberg

Publish with us

Policies and ethics

Search

Navigation