Molecular Mechanisms Regulating Root Hair Tip Growth: A Comparison with Pollen Tubes



The developmental program of roots is constantly modified according to environmental signals and often includes an elevation in the density of root hairs, which increases the root’s absorptive surface in an attempt to meet the ion and water demands of the plant. Root hairs emerge from certain epidermal cells and this depends on a complex genetic cascade. Once this has determined root hair cell fate, local wall loosening and turgor pressure initiate a bulge in the cell wall. The transition from root hair initiation to actual tip growth begins with the accumulation of secretory vesicles at the apical part of the bulge. A complex interplay between ion oscillations, cytoskeleton architecture, vesicle trafficking, cell wall metabolism and hormonal and environmental signals allows the root hair to maintain growth at the tip. This review summarizes the current knowledge on the core components regulating root hair tip growth, critically identifies challenges for future research and points to commonalities and differences with the current knowledge on pollen tube tip growth.


Arabidopsis Calcium Cell wall Cytoskeleton Elongation Pollen tube Root hair ROPs ROS Tip growth 



autoinhibited Ca2+-ATPase




actin-depolymerizing factor


actin filaments


Arabidopsis H+-ATPase







ARP2/3 complex

actin-related protein 2/3 complex


adenosine triphosphatase






1,2-bis(o-aminophenoxy)ethane-N,N,N′,N′-tetraacetic acid


constitutively active


cytoplasmic calcium concentration


endoplasmic reticulum calcium concentration


extracellular calcium concentration




cyclic adenosine monophosphate




calcineurin B-like proteins


carbohydrate-binding module 3a


calcium-dependent protein kinase




CBL-interacting protein kinases


chloride concentration cytoplasmic


calmodulin-like proteins


cortical microtubules


cyclic nucleotide-gated channel


cyclic nucleotide






Cdc42- and Rac-interactive binding


Catharanthus roseus RLK1-like kinases


cellulose synthase complex




cytochalasin B


depolarization-activated calcium channel




dominant negative




ER-type Ca2+-ATPase


ethylene glycol-bis(β-aminoethyl ether)-N,N,N′,N′-tetraacetic acid


endoplasmic microtubules




filamentous actin



FH1 domain

formin homology 1 domain

FH2 domain

formin homology 2 domain


Förster resonance energy transfer


globular actin




GTPase-activating protein


guanosine nucleotide dissociation inhibitor


guanosine diphosphate


guanine nucleotide exchange factor


green fluorescent protein


glutamate receptor


guanosine triphosphate


guanosine triphosphatase


hyperpolarization-activated calcium channel




human embryonic kidney




inositol trisphosphate


latrunculin B


Lycopersicon esculentum phosphate transporter 1








mitochondrial Ca2+ uniporter










myosin-binding proteins 1/2




NADPH oxidase


open reading frame




pleckstrin homology


cytoplasmic pH


extracellular pH






phosphatidylinositol 4-phosphate


phosphatidylinositol 4,5-biphosphate

Plus(+) end

barbed actin filament end


plasma membrane


pectin methylesterase


pectin methylesterase inhibitor


profilin 1


plant-specific ROP nucleotide exchanger


pollen tube


quantitative reverse transcriptase polymerase chain reaction






root hair






root hair specific








receptor-like kinase


RNA interference


Rho-like GTPases from plants


reactive oxygen species








superoxide dismutase


The Arabidopsis Information Resource


























Yellow Cameleon 3.6 (cytosolic calcium sensor)


yellow fluorescent protein


  1. Ahn SJ, Shin R, Schachtman DP (2004) Expression of KT/KUP genes in Arabidopsis and the role of root hairs in K+ uptake. Plant Physiol 134:1135–1145PubMedPubMedCentralCrossRefGoogle Scholar
  2. Akerman KEO, Moore AL (1983) Phosphate dependent, ruthenium red insensitive Ca2+ uptake in mung bean mitochondria. Biochem Biophys Res Commun 114:1176–1181PubMedCrossRefGoogle Scholar
  3. Akkerman M, Franssen-Verheijen MAW, Immerzeel P, Hollander LD, Schel JH, Emons AM (2012) Texture of cellulose microfibrils of root hair cell walls of Arabidopsis thaliana, Medicago truncatula, and Vicia sativa. J Microsc 247:60–67PubMedCrossRefGoogle Scholar
  4. Allen GJ, Sanders D (1996) Control of ionic currents in guard cell vacuoles by cytosolic and luminal calcium. Plant J. 10:1055–1069PubMedCrossRefGoogle Scholar
  5. Allen GJ, Chu SP, Harrington CL, Schumacher K, Hoffmann T, Tang YY, Grill E, Schroeder JI (2001) A defined range of guard cell calcium oscillation parameters encodes stomatal movements. Nature 411:1053–1057PubMedCrossRefGoogle Scholar
  6. Allwood EG, Smertenko AP, Hussey PJ (2001) Phosphorylation of plant actin-depolymerising factor by calmodulin-like domain protein kinase. FEBS Lett 499:97–100PubMedCrossRefGoogle Scholar
  7. 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 14:2915–2927PubMedPubMedCentralCrossRefGoogle Scholar
  8. Almagro L, Gómez Ros LV, Belchi-Navarro S, Bru R, Ros Barceló A, Pedreño MA (2009) Class III peroxidases in plant defence reactions. J Exp Bot 60:377–390PubMedCrossRefGoogle Scholar
  9. An YQ, Huang S, McDowell JM, McKinney EC, Meagher RB (1996a) Conserved expression of the Arabidopsis ACT1 and ACT 3 actin subclass in organ primordia and mature pollen. Plant Cell 8:15–30PubMedPubMedCentralCrossRefGoogle Scholar
  10. An YQ, McDowell JM, Huang S, McKinney EC, Chambliss S, Meagher RB (1996b) Strong, constitutive expression of the Arabidopsis ACT2/ACT8 actin subclass in vegetative tissues. Plant J 10:107–121PubMedCrossRefGoogle Scholar
  11. An R, Chen QJ, Chai MF, Lu PL, Su Z, Qin ZX, Chen J, Wang XC (2007) AtNHX8, a member of the monovalent cation:proton antiporter-1 family in Arabidopsis thaliana, encodes a putative Li+/H+ antiporter. Plant J 49:718–728PubMedCrossRefGoogle Scholar
  12. Andrianantoandro E, Pollard TD (2006) Mechanism of actin filament turnover by severing and nucleation at different concentrations of ADF/cofilin. Mol Cell 24:13–23PubMedCrossRefGoogle Scholar
  13. Arioli T, Peng L, Betzner AS, Burn J, Wittke W, Herth W, Camilleri C, Höfte H, Plazinski J, Birch R, Cork A, Glover J, Redmond J, Williamson RE (1998) Molecular analysis of cellulose biosynthesis in Arabidopsis. Science 279:717–720PubMedCrossRefGoogle Scholar
  14. Ashcroft F, Gadsby D, Miller C (2009) Introduction. The blurred boundary between channels and transporters. Philos Trans R Soc Lond B Biol Sci 364:145–147PubMedCrossRefGoogle Scholar
  15. Augustine RC, Pattavina KA, Tuzel E, Vidali L, Bezanilla M (2011) Actin interacting protein1 and actin depolymerizing factor drive rapid actin dynamics in Physcomitrella patens. Plant Cell 23:3696–3710PubMedPubMedCentralCrossRefGoogle Scholar
  16. 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 150:700–709PubMedPubMedCentralCrossRefGoogle Scholar
  17. Avisar D, Abu-Abied M, Belausov E, Sadot E (2012) Myosin XIK is a major player in cytoplasm dynamics and is regulated by two amino acids in its tail. J Exp Bot 63:241–249PubMedCrossRefGoogle Scholar
  18. Bai L, Ma X, Zhang G, Song S, Zhou Y, Gao L, Miao Y, Song CP (2014a) A receptor-like kinase mediates ammonium homeostasis and is important for the polar growth of root hairs in Arabidopsis. Plant Cell 26:1497–1511PubMedPubMedCentralCrossRefGoogle Scholar
  19. Bai L, Zhou Y, Ma X, Gao L, Song CP (2014b) Arabidopsis CAP1-mediated ammonium sensing required reactive oxygen species in plant cell growth. Plant Signal Behav 9:e29582PubMedCentralCrossRefGoogle Scholar
  20. Balcerowicz D, Schoenaers S, Vissenberg K (2015) Cell fate determination and the switch from diffuse growth to planar polarity in arabidopsis root epidermal cells. Front Plant Sci 6:1–13CrossRefGoogle Scholar
  21. Baluška 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 227:618–632PubMedCrossRefGoogle Scholar
  22. 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 28:145–157PubMedCrossRefGoogle Scholar
  23. Baskin TI, Betzner AS, Hoggart R, Cork A, Williamson RE (1992) Root morphology mutants in Arabidopsis thaliana. Aust J Plant Physiol 19:427–437CrossRefGoogle Scholar
  24. Bates TR, Lynch JP (1996) Stimulation of root hair elongation in Arabidopsis thaliana by low phosphorus availability. Plant Cell Environ 19:529–538CrossRefGoogle Scholar
  25. Battey NH, Blackbourn HD (1993) The control of exocytosis in plant cells. New Phytol 125:307–338CrossRefGoogle Scholar
  26. Battey NH, James NC, Greenland AJ, Brownlee C (1999) Exocytosis and endocytosis. Plant Cell 11:643–659PubMedPubMedCentralCrossRefGoogle Scholar
  27. Baumberger N, Ringli C, Keller B (2001) The chimeric leucine-rich repeat/extensin cell wall protein LRX1 is required for root hair morphogenesis in Arabidopsis thaliana. Genes Dev 15:1128–1139PubMedPubMedCentralCrossRefGoogle Scholar
  28. Becker JD, Takeda S, Borges F, Dolan L, Feijó JA (2014) Transcriptional profiling of Arabidopsis root hairs and pollen defines an apical cell growth signature. BMC Plant Biol 14:197PubMedPubMedCentralCrossRefGoogle Scholar
  29. Berken A, Thomas C, Wittinghofer A (2005) A new family of RhoGEFs activates the Rop molecular switch in plants. Nature 436:1176–1180PubMedCrossRefGoogle Scholar
  30. Bernal AJ, Yoo C-M, Mutwil M, Jensen JK, Hou G, Blaukopf C, Sørensen I, Blancaflor EB, Scheller HV, Willats WG (2008) Functional analysis of the cellulose synthase-like genes CSLD1, CSLD2, and CSLD4 in tip-growing Arabidopsis cells. Plant Physiol 148:1238–1253PubMedPubMedCentralCrossRefGoogle Scholar
  31. Bibikova TN, Zhigilei A, Gilroy S (1997) Root hair growth in Arabidopsis thaliana is directed by calcium and an endogenous polarity. Planta 203:495–505PubMedCrossRefGoogle Scholar
  32. 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
  33. Bibikova TN, Blancaflor EB, Gilroy S (1999) Microtubules regulate tip growth and orientation in root hairs of Arabidopsis thaliana. Plant J 17:657–665PubMedCrossRefGoogle Scholar
  34. Bienert GP, Møller AL, Kristiansen KA, Schulz A, Møller IM, Schjoerring JK, Jahn TP (2007) Specific aquaporins facilitate the diffusion of hydrogen peroxide across membranes. J Biol Chem 282(2):1183–1192PubMedCrossRefGoogle Scholar
  35. Bischoff F, Vahlkamp L, Molendijk A, Palme K (2000) Localization of AtROP4 and AtROP6 and interaction with the guanine nucleotide dissociation inhibitor AtRhoGDI1 from Arabidopsis. Plant Mol Biol 42:515–530PubMedCrossRefGoogle Scholar
  36. Boavida LC, McCormick S (2007) Temperature as a determinant factor for increased and reproducible in vitro pollen germination in Arabidopsis thaliana. Plant J 52:570–582PubMedCrossRefGoogle Scholar
  37. Bock KW, Honys D, Ward JM, Padmanaban S, Nawrocki EP, Hirschi KD, Twell D, Sze H (2006) Integrating membrane transport with male gametophyte development and function through transcriptomics. Plant Physiol 140:1151–1168PubMedPubMedCentralCrossRefGoogle Scholar
  38. Boisson-Dernier A, Roy S, Kritsas K, Grobei MA, Jaciubek M, Schroeder JI, Grossniklaus U (2009) Disruption of the pollen-expressed FERONIA homologs ANXUR1 and ANXUR2 triggers pollen tube discharge. Development 136:3279–3288PubMedPubMedCentralCrossRefGoogle Scholar
  39. Boisson-Dernier A, Lituiev DS, Nestorova A, Franck CM, Thirugnanarajah S, Grossniklaus U (2013) ANXUR receptor-like kinases coordinate cell wall integrity with growth at the pollen tube tip via NADPH oxidases. PLoS Biol 11:e1001719PubMedPubMedCentralCrossRefGoogle Scholar
  40. Boron AK, Van Orden J, Nektarios Markakis M, Mouille G, Adriaensen D, Verbelen JP, Höfte H, Vissenberg K (2014) Proline-rich protein-like PRPL1 controls elongation of root hairs in Arabidopsis thaliana. J Exp Bot 65:5485–5495PubMedPubMedCentralCrossRefGoogle Scholar
  41. Bosch M, Hepler PK (2005) Pectin methylesterases and pectin dynamics in pollen tubes. Plant Cell Online 17:3219–3226CrossRefGoogle Scholar
  42. Bou Daher F, Geitmann A (2011) Actin is involved in pollen tube tropism through redefining the spatial targeting of secretory vesicles. Traffic 12:1537–1551PubMedCrossRefGoogle Scholar
  43. Bou Daher F, Van Oostende C, Geitmann A (2011) Spatial and temporal expression of actin depolymerizing factors ADF7 and ADF10 during male gametophyte development in Arabidopsis thaliana. Plant Cell Physiol 52:1177–1192PubMedCrossRefGoogle Scholar
  44. Brady SM, Orlando DA, Lee J-Y, Wang JY, Koch J, Dinneny JR, Mace D, Ohler U, Benfey PN (2007) A high-resolution root spatiotemporal map reveals dominant expression patterns. Science 318:801–806PubMedCrossRefGoogle Scholar
  45. Braun M, Baluška F, Von Witsch M, Menzel D (1999) Redistribution of actin, profilin and phosphatidylinositol-4,5-bisphosphate in growing and maturing root hairs. Planta 209:435–443PubMedCrossRefGoogle Scholar
  46. Braun M, Hauslage J, Czogalla A, Limbach C (2004) Tip-localized actin polymerization and remodeling, reflected by the localization of ADF, profilin and villin, are fundamental for gravity-sensing and polar growth in characean rhizoids. Planta 219:379–388PubMedCrossRefGoogle Scholar
  47. Britto DT, Kronzucker HJ (2002) NH4+ toxicity in higher plants: a critical review. J Plant Physiol 159:567–584CrossRefGoogle Scholar
  48. Bruex A, Kainkaryam RM, Wieckowski Y, Kang YH, Bernhardt C, Xia Y, Zheng X, Wang JY, Lee MM, Benfey P, Woolf PJ, Schiefelbein J (2012) A gene regulatory network for root epidermis cell differentiation in Arabidopsis. PLoS Genet 8:e1002446PubMedPubMedCentralCrossRefGoogle Scholar
  49. Bush DS (1995) Calcium regulation in plant cells and its role in signaling. Annu Rev Plant Physiol Plant Mol Biol 46:95–122CrossRefGoogle Scholar
  50. Cárdenas L (2009) New findings in the mechanisms regulating polar growth in root hair cells. Plant Signal Behav 4:4–8PubMedPubMedCentralCrossRefGoogle Scholar
  51. Cárdenas L, Lovy-Wheeler A, Kunkel JG, Hepler PK (2008) Pollen tube growth oscillations and intracellular calcium levels are reversibly modulated by actin polymerization. Plant Phys 146:1611–1621CrossRefGoogle Scholar
  52. Carol RJ, Dolan L (2002) Building a hair: tip growth in Arabidopsis thaliana root hairs. Philos Trans R Soc Lond B Biol Sci 357:815–821PubMedPubMedCentralCrossRefGoogle Scholar
  53. 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
  54. Carpita NC, Gibeaut DM (1993) Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant J 3:1–30PubMedCrossRefGoogle Scholar
  55. Cavalier DM, Lerouxel O, Neumetzler L, Yamauchi K, Reinecke A, Freshour G, Zabotina OA, Hahn MG, Burgert I, Pauly M, Raikhel NV, Keegstra K (2008) Disrupting two Arabidopsis thaliana xylosyltransferase genes results in plants deficient in xyloglucan, a major primary cell wall component. Plant Cell 20:1519–1537PubMedPubMedCentralCrossRefGoogle Scholar
  56. Certal AC, Almeida RB, Carvalho LM, Wong E, Moreno N, Michard E, Carneiro J, Rodriguéz-Léon J, Wu HM, Cheung AY, Feijó JA (2008) Exclusion of a proton ATPase from the apical membrane is associated with cell polarity and tip growth in Nicotiana tabacum pollen tubes. Plant Cell 20:614–634PubMedPubMedCentralCrossRefGoogle Scholar
  57. Chang M, Huang S (2015) Arabidopsis ACT11 modifies actin turnover to promote pollen germination and maintain the normal rate of tube growth. Plant J 83:515–527PubMedCrossRefGoogle Scholar
  58. Chang F, Gu Y, Ma H, Yang Z (2013) AtPRK2 promotes ROP1 activation via RopGEFs in the control of polarized pollen tube growth. Mol Plant 6:1187–1201PubMedCrossRefGoogle Scholar
  59. Chebli Y, Kaneda M, Zerzour R, Geitmann A (2012) The cell wall of the Arabidopsis pollen tube-spatial distribution, recycling, and network formation of polysaccharides. Plant Physiol 160:1940–1955PubMedPubMedCentralCrossRefGoogle Scholar
  60. Chen CY, Wong EI, Vidali L, Estavillo A, Hepler PK, Wu HM, Cheung AY (2002) The regulation of actin organization by actin-depolymerizing factor in elongating pollen tubes. Plant Cell 14:2175–2190PubMedPubMedCentralCrossRefGoogle Scholar
  61. Chen CY, Cheung AY, Wu H (2003) Actin-depolymerizing factor mediates Rac/Rop GTPase–regulated pollen tube growth. Society 15:237–249Google Scholar
  62. Cheung AY, Niroomand S, Zou Y, Wu H-M (2010) A transmembrane formin nucleates subapical actin assembly and controls tip-focused growth in pollen tubes. Proc Natl Acad Sci USA 107:16390–16395PubMedPubMedCentralCrossRefGoogle Scholar
  63. Choi WG, Swanson SJ, Gilroy S (2012) High-resolution imaging of Ca2+, redox status, ROS and pH using GFP biosensors. Plant J 70:118–128PubMedCrossRefGoogle Scholar
  64. Choi W-G, Toyota M, Kim S-H, Hilleary R, Gilroy S (2014) Salt stress-induced Ca2+ waves are associated with rapid, long-distance root-to-shoot signaling in plants. Proc Natl Acad Sci USA 111(17):6497–6502PubMedPubMedCentralCrossRefGoogle Scholar
  65. Cole RA, Fowler JE (2006) Polarized growth: maintaining focus on the tip. Curr Opin Plant Biol 9:579–588PubMedCrossRefGoogle Scholar
  66. Cosgrove DJ (2000) Loosening of plant cell walls by expansins. Nature 407:321–326PubMedCrossRefGoogle Scholar
  67. Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6:850–861PubMedCrossRefGoogle Scholar
  68. Cvrckova F, Novotny M, Pickova D, Zarsky V (2004) Formin homology 2 domains occur in multiple contexts in angiosperms. BMC Genomics 5:44PubMedPubMedCentralCrossRefGoogle Scholar
  69. Dadacz-Narloch B, Beyhl D, Larisch C, López-Sanjurjo EJ, Reski R, Kuchitsu K, Müller TD, Becker D, Schönknecht G, Hedrich R (2011) A novel calcium binding site in the slow vacuolar cation channel TPC1 senses luminal calcium levels. Plant Cell 23:2696–2707PubMedPubMedCentralCrossRefGoogle Scholar
  70. Daram P, Brunner S, Persson BL, Amrhein N, Bucher M (1998) Functional analysis and cell-specific expression of a phosphate transporter from tomato. Planta 206:225–233PubMedCrossRefGoogle Scholar
  71. Day IS, Reddy VS, Ali GS, Reddy ASN (2002) Analysis of EF-hand-containing proteins in Arabidopsis. Genome Biol 3:10CrossRefGoogle Scholar
  72. Deeks MJ, Hussey PJ, Davies B (2002) Formins: intermediates in signal-transduction cascades that affect cytoskeletal reorganization. Trends Plant Sci 7:492–498PubMedCrossRefGoogle Scholar
  73. Deeks MJ, Cvrcková F, Machesky LM, Mikitová V, Ketelaar T, Zársky 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 168:529–540PubMedCrossRefGoogle Scholar
  74. Deeks MJ, Fendrych M, Smertenko A, Bell KS, Oparka K, Cvrcková F, Zársky V, Hussey PJ (2010) The plant formin AtFH4 interacts with both actin and microtubules, and contains a newly identified microtubule-binding domain. J Cell Sci 123:1209–1215PubMedCrossRefGoogle Scholar
  75. Demidchik V, Bowen HC, Maathuis FJM, Shabala SN, Tester MA, White PJ, Davies JM (2002) Arabidopsis thaliana root non-selective cation channels mediate calcium uptake and are involved in growth. Plant J 32:799–808PubMedCrossRefGoogle Scholar
  76. DerMardirossian C, Bokoch GM (2005) GDIs: central regulatory molecules in Rho GTPase activation. Trends Cell Biol 15:356–363PubMedCrossRefGoogle Scholar
  77. Desbrosses G, Josefsson C, Rigas S, Hatzopoulos P, Dolan L (2003) AKT1 and TRH1 are required during root hair elongation in Arabidopsis. J Exp Bot 54:781–788PubMedCrossRefGoogle Scholar
  78. Di Giorgio JP, Bienert GP, Ayub N, Yaneff A, Barberini ML, Mecchia MA, Amodeo G, Soto GC, Muschietti JP (2016) Pollen-specific aquaporins NIP4;1 and NIP4;2 are required for pollen development and pollination in Arabidopsis thaliana. Plant Cell 28(5):1053–1077PubMedPubMedCentralCrossRefGoogle Scholar
  79. Dick-Pérez M, Zhang Y, Hayes J, Salazar A, Zabotina OA, Hong M (2011) Structure and interactions of plant cell-wall polysaccharides by two- and three-dimensional magic-angle-spinning solid-state NMR. Biochemistry 50:989–1000PubMedCrossRefGoogle Scholar
  80. Diet A, Brunner S, Ringli C (2004) The enl mutants enhance the lrx1 root hair mutant phenotype of Arabidopsis thaliana. Plant Cell Physiol 45:734–741PubMedCrossRefGoogle Scholar
  81. Diet A, Link B, Seifert GJ, Schellenberg B, Wagner U, Pauly M, Reiter WD, Ringli C (2006) The Arabidopsis root hair cell wall formation mutant lrx1 is suppressed by mutations in the RHM1 gene encoding a UDP-L-rhamnose synthase. Plant Cell 18:1630–1641PubMedPubMedCentralCrossRefGoogle Scholar
  82. Dieter P, Marmé D (1980) Ca2+ transport in mitochondrial and microsomal fractions from higher plants. Planta 150:1–8PubMedCrossRefGoogle Scholar
  83. Doblin MS, Kurek I, Jacob-Wilk D, Delmer DP (2002) Cellulose biosynthesis in plants: from genes to rosettes. Plant Cell Physiol 43:1407–1420PubMedCrossRefGoogle Scholar
  84. Dodd AN, Kudla J, Sanders D (2010) The language of calcium signaling. Annu Rev Plant Biol 61:593–620PubMedCrossRefGoogle Scholar
  85. Dong CH, Hong Y (2013) Arabidopsis CDPK6 phosphorylates ADF1 at N-terminal serine 6 predominantly. Plant Cell Rep 32:1715–1728PubMedCrossRefGoogle Scholar
  86. Dong CH, Kost B, Xia G, Chua NH (2001a) Molecular identification and characterization of the Arabidopsis AtADF1, AtADFS and AtADF6 genes. Plant Mol Biol 45:517–527PubMedCrossRefGoogle Scholar
  87. Dong CH, Xia GX, Hong Y, Ramachandran S, Kost B, Chua NH (2001b) ADF proteins are involved in the control of flowering and regulate F-actin organization, cell expansion, and organ growth in Arabidopsis. Plant Cell 13:1333–1346PubMedPubMedCentralCrossRefGoogle Scholar
  88. Drerup MM, Schlücking K, Hashimoto K, Manishankar P, Steinhorst L, Kuchitsu K, Kudla J (2013) The calcineurin B-like calcium sensors CBL1 and CBL9 together with their interacting protein kinase CIPK26 regulate the Arabidopsis NADPH oxidase RBOHF. Mol Plant 6:559–569PubMedCrossRefGoogle Scholar
  89. Duan Q, Kita D, Li C, Cheung AY, Wu HM (2010) FERONIA receptor-like kinase regulates RHO GTPase signaling of root hair development. Proc Natl Acad Sci USA 107:17821–17826PubMedPubMedCentralCrossRefGoogle Scholar
  90. Duan Q, Kita D, Johnson E, Aggarwal M, Gates L, Wu HM, Cheung AY (2014) Reactive oxygen species mediate pollen tube rupture to release sperm for fertilization in Arabidopsis. Nat Commun 5:3129PubMedGoogle Scholar
  91. Dubiella U, Seybold H, Durian G, Komander E, Lassig R, Witte CP, Schulze WX, Romeis T (2013) Calcium-dependent protein kinase/NADPH oxidase activation circuit is required for rapid defense signal propagation. Proc Natl Acad Sci USA 110:8744–8749PubMedPubMedCentralCrossRefGoogle Scholar
  92. Dutta R, Robinson KR (2004) Identification and characterization of stretch-activated ion channels in pollen protoplasts. Plant Physiol 135:1398–1406PubMedPubMedCentralCrossRefGoogle Scholar
  93. Emons AMC, van Maaren N (1987) Helicoidal cell-wall texture in root hairs. Planta 170:145–151PubMedCrossRefGoogle Scholar
  94. Eng RC, Wasteneys GO (2014) The microtubule plus-end tracking protein ARMADILLO-REPEAT KINESIN1 promotes microtubule catastrophe in Arabidopsis. Plant Cell 26:3372–3386PubMedPubMedCentralCrossRefGoogle Scholar
  95. Escobar-Restrepo J, Huck N, Kessler S, Gagliardini V, Gheyselinck J, Yang WC, Grossniklaus U (2007) The FERONIA receptor-like kinase mediates male-female interactions during pollen tube reception. Science 317:656–660PubMedCrossRefGoogle Scholar
  96. Estruch JJ, Kadwell S, Merlin E, Crossland L (1994) Cloning and characterization of a maize pollen-specific calcium-dependent calmodulin-independent protein kinase. Proc Natl Acad Sci USA 91:8837–8841PubMedPubMedCentralCrossRefGoogle Scholar
  97. Evans NH, McAinsh MR, Hetherington AM (2001) Calcium oscillations in higher plants. Curr Opin Plant Biol 4:415–420PubMedCrossRefGoogle Scholar
  98. Fagard M, Desnos T, Desprez T, Goubet F, Refregier G, Mouille G, McCann M, Rayon C, Vernhettes S, Höfte H (2000) PROCUSTE1 encodes a cellulose synthase required for normal cell elongation specifically in roots and dark-grown hypocotyls of Arabidopsis. Plant Cell 12:2409–2424PubMedPubMedCentralCrossRefGoogle Scholar
  99. Fan JL, Wei XZ, Wan LC, Zhang LY, Zhao XQ, Liu WZ, Hao HQ, Zhang HY (2011) Disarrangement of actin filaments and Ca2+ gradient by CdCl2 alters cell wall construction in Arabidopsis thaliana root hairs by inhibiting vesicular trafficking. J Plant Physiol 168:1157–1167PubMedCrossRefGoogle Scholar
  100. Favery B, Ryan E, Foreman J, Linstead P, Boudonck K, Steer M, Shaw P, Dolan L (2001) KOJAK encodes a cellulose synthase-like protein required for root hair cell morphogenesis in Arabidopsis. Genes Dev 15:79–89PubMedPubMedCentralCrossRefGoogle Scholar
  101. Feijó J, Malho R, Pais M (1992) A cytochemical study on the role of atpases during pollen germination in Agapanthus umbellatus. Sex Plant Reprod 5:138–145CrossRefGoogle Scholar
  102. Feijó JA, Sainhas J, Hackett GR, Kunkel JG, Hepler PK (1999) Growing pollen tubes possess a constitutive alkaline band in the clear zone and a growth-dependent acidic tip. J Cell Biol 144:483–496PubMedPubMedCentralCrossRefGoogle Scholar
  103. Felle HH (1994) The H+/Cl- symporter in root-hair cells of Sinapis alba (an electrophysiological study using ion-selective microelectrodes). Plant Physiol 106:1131–1136PubMedPubMedCentralCrossRefGoogle Scholar
  104. Felle HH (2001) pH: signal and messenger in plant cells. Plant Biol 3:577–591CrossRefGoogle Scholar
  105. 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 114:39–45PubMedPubMedCentralCrossRefGoogle Scholar
  106. Feng Q-N, Kang H, Song SJ, Ge FR, Zhang YL, Li E, Li S, Zhang Y (2016) Arabidopsis RhoGDIs are critical for cellular homeostasis of pollen tubes. Plant Physiol 170:841–856PubMedCrossRefGoogle Scholar
  107. 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 422:442–446PubMedCrossRefGoogle Scholar
  108. Franklin-Tong V (1999) Signaling and the modulation of pollen tube growth. Plant Cell 11:727–738PubMedPubMedCentralCrossRefGoogle Scholar
  109. Fricker MD, White NS, Obermeyer G (1997) pH gradients are not associated with tip growth in pollen tubes of Lilium longiflorum. J Cell Sci 110:1729–1740PubMedGoogle Scholar
  110. Frietsch S, Wang Y-F, Sladek C, Poulsen LR, Romanowsky SM, Schroeder JI, Harper JF (2007) A cyclic nucleotide-gated channel is essential for polarized tip growth of pollen. Proc Natl Acad Sci USA 104:14531–14536PubMedPubMedCentralCrossRefGoogle Scholar
  111. Fry SC (1998) Oxidative scission of plant cell wall polysaccharides by ascorbate-induced hydroxyl radicals. Biochem J 332:507–515PubMedPubMedCentralCrossRefGoogle Scholar
  112. 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 152:1019–1032PubMedPubMedCentralCrossRefGoogle Scholar
  113. 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
  114. Fu Y, Xu T, Zhu L, Wen M, Yang Z (2009) A ROP gtpase signaling pathway controls cortical microtubule ordering and cell expansion in Arabidopsis. Curr Biol 19:1827–1832PubMedPubMedCentralCrossRefGoogle Scholar
  115. Fuglsang AT, Guo Y, Cuin TA, Qiu Q, Song C, Kristiansen KA, Bych K, Schulz A, Shabala S, Schumaker KS, Palmgren MG, Zhu JK (2007) Arabidopsis protein kinase PKS5 inhibits the plasma membrane H+ -ATPase by preventing interaction with 14-3-3 protein. Plant Cell 19:1617–1634PubMedPubMedCentralCrossRefGoogle Scholar
  116. Galway ME, Eng RC, Schiefelbein JW, Wasteneys GO (2011) Root hair-specific disruption of cellulose and xyloglucan in AtCSLD3 mutants, and factors affecting the post-rupture resumption of mutant root hair growth. Planta 233:985–999PubMedCrossRefGoogle Scholar
  117. García-Hernández EDR, Cassab López GI (2005) Structural cell wall proteins from five pollen species and their relationship with boron. Braz J Plant Physiol 17:375–381CrossRefGoogle Scholar
  118. Gao QF, Gu LL, Wang HQ, Fei CF, Fang X, Hussain J, Sun SJ, Dong JY, Liu H, Wang YF (2016) Cyclic nucleotide-gated channel 18 is an essential Ca2+ channel in pollen tube tips for pollen tube guidance to ovules in Arabidopsis. Proc Natl Acad Sci USA 113:3096–3101PubMedPubMedCentralCrossRefGoogle Scholar
  119. Gibbon BC, Zonia LE, Kovar DR, Hussey PJ, Staiger CJ (1998) Pollen profilin function depends on interaction with proline-rich motifs. Plant Cell 10:981–993PubMedPubMedCentralCrossRefGoogle Scholar
  120. Gibbon BC, Kovar DR, Staiger CJ (1999) Latrunculin B has different effects on pollen germination and tube growth. Plant Cell 11:2349–2363PubMedPubMedCentralCrossRefGoogle Scholar
  121. 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 130:2199–2209PubMedPubMedCentralCrossRefGoogle Scholar
  122. Gilroy S, Jones DL (2000) Through form to function: root hair development and nutrient uptake. Trends Plant Sci 5:56–60PubMedCrossRefGoogle Scholar
  123. Gjetting KSK, Ytting CK, Schulz A, Fuglsang AT (2012) Live imaging of intra- and extracellular pH in plants using pHusion, a novel genetically encoded biosensor. J Exp Bot 63:3207–3218PubMedPubMedCentralCrossRefGoogle Scholar
  124. Gossot O, Geitmann A (2007) Pollen tube growth: coping with mechanical obstacles involves the cytoskeleton. Planta 226:405–416PubMedCrossRefGoogle Scholar
  125. Griessner M, Obermeyer G (2003) Characterization of whole-cell K + currents across the plasma membrane of pollen grain and tube protoplasts of Lilium longiflorum. J Membr Biol 193:99–108PubMedCrossRefGoogle Scholar
  126. Gu Y, Vernoud V, Fu Y, Yang Z (2003) ROP GTPase regulation of pollen tube growth through the dynamics of tip-localized F-actin. J Exp Bot 54:93–101PubMedCrossRefGoogle Scholar
  127. 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 169:127–138PubMedPubMedCentralCrossRefGoogle Scholar
  128. Gu Y, Li S, Lord E, Yang Z (2006) Members of a novel class of Arabidopsis Rho guanine nucleotide exchange factors control Rho GTPase-dependent polar growth. Plant Cell 18:366–381PubMedPubMedCentralCrossRefGoogle Scholar
  129. Guan Y, Lu J, Xu J, McClure B, Zhang S (2014) Two mitogen-activated protein kinases, MPK3 and MPK6, are required for funicular guidance of pollen tubes in Arabidopsis. Plant Physiol 165:528–533PubMedPubMedCentralCrossRefGoogle Scholar
  130. Gungabissoon RA, Jiang CJ, Drøbak BK, Maciver SK, Hussey PJ (1998) Interaction of maize actin-depolymerising factor with actin and phosphoinositides and its inhibition of plant phospholipase C. Plant J 16:689–696CrossRefGoogle Scholar
  131. Guo H, Li L, Ye H, Yu X, Algreen A, Yin Y (2009) Three related receptor-like kinases are required for optimal cell elongation in Arabidopsis thaliana. Proc Natl Acad Sci USA 106(18):7648–7653PubMedPubMedCentralCrossRefGoogle Scholar
  132. Gutermuth T, Lassig R, Portes M, Maierhofer T, Romeis T, Borst JW, Hedrich R, Feijó JA, Konrad KR (2013) Pollen tube growth regulation by free anions depends on the interaction between the anion channel SLAH3 and calcium-dependent protein kinases CPK2 and CPK20. Plant Cell 25:4525–4543PubMedPubMedCentralCrossRefGoogle Scholar
  133. Halliwell B, Gutteridge J (1999) Free radical in biology and medicine. Oxford University Press, Oxford, UKGoogle Scholar
  134. Hamam AM, Britto DT, Flam-Shepherd R, Kronzucker HJ (2016) Measurement of differential Na+ efflux from apical and bulk root zones of intact barley and Arabidopsis plants. Front Plant Sci 7:1–8CrossRefGoogle Scholar
  135. Hamilton ES, Jensen GS, Maksaev G, Katims A, Sherp AM, Haswell ES (2015) Mechanosensitive channel MSL8 regulates osmotic forces during pollen hydration and germination. Science 350:438–441PubMedPubMedCentralCrossRefGoogle Scholar
  136. Hanson JB, Malhotra SS, Stoner CD (1965) Action of calcium on corn mitochondrial. Plant Physiol 40:1033–1040PubMedPubMedCentralCrossRefGoogle Scholar
  137. Harlan J, Hajduk P, Yoon H, Fesik S (1994) Pleckstrin homology domains bind to phosphatidylinositol-4,5-bisphosphate. Nature 371:168–170PubMedCrossRefGoogle Scholar
  138. Haruta M, Sabat G, Stecker K, Minkoff BB, Sussman MR (2014) A peptide hormone and its receptor protein kinase regulate plant cell expansion. Science 343:408–411PubMedPubMedCentralCrossRefGoogle Scholar
  139. Hashimoto K, Igarashi H, Mano S, Nishimura M, Shimmen T, Yokota E (2005) Peroxisomal localization of a myosin XI isoform in Arabidopsis thaliana. Plant Cell Physiol 46:782–789PubMedCrossRefGoogle Scholar
  140. Hazak O, Bloch D, Poraty L, Sternberg H, Zhang J, Friml J, Yalovsky S (2010) A Rho scaffold integrates the secretory system with feedback mechanisms in regulation of auxin distribution. PLoS Biol 8(1):e1000282PubMedPubMedCentralCrossRefGoogle Scholar
  141. He X, Liu YM, Wang W, Li Y (2006) Distribution of G-actin is related to root hair growth of wheat. Ann Bot 98:49–55PubMedPubMedCentralCrossRefGoogle Scholar
  142. Heazlewood JL, Tonti-filippini JS, Gout AM, Day DA, Whelan J, Millar AH (2004) Experimental analysis of the Arabidopsis mitochondrial proteome highlights signaling and regulatory components, provides assessment of targeting prediction programs, and indicates plant-specific mitochondrial proteins. Plant Cell 16:241–256PubMedPubMedCentralCrossRefGoogle Scholar
  143. Hedrich R, Marten I (2011) TPC1 - SV channels gain shape. Mol Plant 4:428–441PubMedCrossRefGoogle Scholar
  144. Hepler PK, Kunkel JG, Rounds CM, Winship LJ (2012) Calcium entry into pollen tubes. Trends Plant Sci 17:32–38PubMedCrossRefGoogle Scholar
  145. Herrmann A, Felle H (1995) Tip growth in root hair cells of Sinapis alba L.: significance of internal and external Ca2+ and pH. New Phytol 129:523–533CrossRefGoogle Scholar
  146. Hetherington AM, Brownlee C (2004) The generation of Ca2+ signals in plants. Annu Rev Plant Biol 55:401–427PubMedCrossRefGoogle Scholar
  147. Hohl M, Greiner H, Schopfer P (1995) The cryptic-growth response of maize coleoptiles and its relationship to H2O2-dependent cell wall stiffening. Physiol Plant 94:491–498CrossRefGoogle Scholar
  148. Holdaway-Clarke TL, Hepler PK (2003) Control of pollen tube growth: role of ion gradients and fluxes. New Phytol 159:539–563CrossRefGoogle Scholar
  149. Holdaway-clarke TL, Feijó JA, Hackett GR, Kunkel JG, Hepler PK (1997) Pollen tube growth and the intracellular cytosolic calcium gradient oscillate in phase while extracellular calcium influx 1 s delayed. Plant Cell 9:1999–2010PubMedPubMedCentralCrossRefGoogle Scholar
  150. Hong D, Jeon BW, Kim SY, Hwang JU, Lee Y (2015) The ROP2-RIC7 pathway negatively regulates light-induced stomatal opening by inhibiting exocyst subunit Exo70B1 in Arabidopsis. New Phytol 209(2):624–635PubMedCrossRefGoogle Scholar
  151. van der Honing HS, Kieft H, Emons AMC, Ketelaar T (2012) Arabidopsis VILLIN2 and VILLIN3 are required for the generation of thick actin filament bundles and for directional organ growth. Plant Physiol 158:1426–1438PubMedCrossRefGoogle Scholar
  152. Hooijmaijers C, Rhee JY, Kwak KJ, Chung GC, Horie T, Katsuhara M, Kang H (2012) Hydrogen peroxide permeability of plasma membrane aquaporins or Arabidopsis thaliana. J Plant Res 125(1):147–153PubMedCrossRefGoogle Scholar
  153. Huang S, McDowell JM, Weise MJ, Meagher RB (1996) The Arabidopsis profilin gene family. Evidence for an ancient split between constitutive and pollen-specific profilin genes. Plant Physiol 111:115–126PubMedPubMedCentralCrossRefGoogle Scholar
  154. Huang SH, An Y-Q, McDowell JM, McKinney EC, Meagher RB (1997) The Arabidopsis ACT11 actin gene is strongly expressed in tissues of the emerging inflorescence, pollen, and developing ovules. Plant Mol Biol 33:125–139PubMedCrossRefGoogle Scholar
  155. Huang S, Robinson RC, Gao LY, Matsumoto T, Brunet A, Blanchoin L, Staiger CJ (2005) Arabidopsis VILLIN1 generates actin filament cables that are resistant to depolymerization. Plant Cell 17:486–501PubMedPubMedCentralCrossRefGoogle Scholar
  156. Huang G-Q, Li E, Ge F-R, Li S, Wang Q, Zhang CQ, Zhang Y (2013a) Arabidopsis RopGEF4 and RopGEF10 are important for FERONIA-mediated developmental but not environmental regulation of root hair growth. New Phytol 200:1089–1101PubMedCrossRefGoogle Scholar
  157. Huang J, Kim CM, Xuan YH, Liu J, Kim TH, Kim BK, Han CD (2013b) Formin homology 1 (OsFH1) regulates root-hair elongation in rice (Oryza sativa). Planta 237:1227–1239PubMedCrossRefGoogle Scholar
  158. Hussey PJ, Ketelaar T, Deeks MJ (2006) Control of the actin cytoskeleton in plant cell growth. Annu Rev Plant Biol 57:109–125PubMedCrossRefGoogle Scholar
  159. Hwang J-U, Vernoud V, Szumlanski A, Nielsen E, Yang Z (2008) A tip-localized Rho GTPase-activating protein controls cell polarity by globally inhibiting Rho GTPase at the cell apex. Curr Biol 18:1907–1916PubMedPubMedCentralCrossRefGoogle Scholar
  160. Hwang J-U, Wu G, Yan A, Lee YJ, Grierson CS, Yang Z (2010) Pollen-tube tip growth requires a balance of lateral propagation and global inhibition of Rho-family GTPase activity. J Cell Sci 123:340–350PubMedPubMedCentralCrossRefGoogle Scholar
  161. Idilli A, Onelli E, Moscatelli A (2012) Low concentration of LatB dramatically changes the microtubule organization and the timing of vegetative nucleus/generative cell entrance in tobacco pollen tubes. Plant Signal Behav 7:947–950PubMedPubMedCentralCrossRefGoogle Scholar
  162. Isayenkov S, Isner JC, Maathuis FJM (2010) Vacuolar ion channels: roles in plant nutrition and signalling. FEBS Lett 584:1982–1988PubMedCrossRefGoogle Scholar
  163. Ivashikina N, Becker D, Ache P, Meyerhoff O, Felle HH, Hedrich R (2001) K+ channel profile and electrical properties of Arabidopsis root hairs. FEBS Lett 508:463–469PubMedCrossRefGoogle Scholar
  164. Ivashuta S, Liu J, Lohar D (2005) RNA interference identifies a calcium-dependent protein kinase involved in Medicago truncatula root development. Plant Cell 17:1–11CrossRefGoogle Scholar
  165. Iwano M, Entani T, Shiba H, Kakita M, Nagai T, Mizuno H, Miyawaki A, Shoji T, Kubo K, Isogai A, Takayama S (2009) Fine-tuning of the cytoplasmic Ca2+ concentration is essential for pollen tube growth. Plant Physiol 150:1322–1334PubMedPubMedCentralCrossRefGoogle Scholar
  166. Jiang L, Yang S-L, Xie L-F, Puah CS, Zhang XQ, Yang WC, Sundaresan V, Ye D (2005) VANGUARD1 encodes a pectin methylesterase that enhances pollen tube growth in the Arabidopsis style and transmitting tract. Plant Cell 17:584–596PubMedPubMedCentralCrossRefGoogle Scholar
  167. Jones D, Shaff J, Kochian L (1995) Role of calcium and other ions in directing root hair tip growth in Limnobium stoloniferum. Planta 197:672–680CrossRefGoogle Scholar
  168. 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 14:763–776PubMedPubMedCentralCrossRefGoogle Scholar
  169. Jones MA, Raymond MJ, Smirnoff N (2006) Analysis of the root-hair morphogenesis transcriptome reveals the molecular identity of six genes with roles in root-hair development in Arabidopsis. Plant J 45:83–100PubMedCrossRefGoogle Scholar
  170. Jones MA, Raymond MJ, Yang Z, Smirnoff N (2007) NADPH oxidase-dependent reactive oxygen species formation required for root hair growth depends on ROP GTPase. J Exp Bot 58:1261–1270PubMedCrossRefGoogle Scholar
  171. Kandasamy MK, Gilliland LU, McKinney EC, Meagher RB (2001) One plant actin isovariant, ACT7, is induced by auxin and required for normal callus formation. Plant Cell 13:1541–1554PubMedPubMedCentralCrossRefGoogle Scholar
  172. Kandasamy MK, McKinney EC, Meagher RB (2002) Functional nonequivalency of actin isovariants in Arabidopsis. Mol Biol Cell 13:251–261PubMedPubMedCentralCrossRefGoogle Scholar
  173. Kandasamy MK, Burgos-Rivera B, McKinney EC, Ruzicka DR, Meagher RB (2007) Class-specific interaction of profilin and ADF isovariants with actin in the regulation of plant development. Plant Cell 19:3111–3126PubMedPubMedCentralCrossRefGoogle Scholar
  174. 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 21:701–718PubMedPubMedCentralCrossRefGoogle Scholar
  175. Kaya H, Nakajima R, Iwano M, Kanaoka MM, Kimura S, Takeda S, Kawarazaki T, Senzaki E, Hamamura Y, Higashiyama T, Takayama S, Abe M, Kuchitsu K (2014) Ca2+-activated reactive oxygen species production by Arabidopsis RbohH and RbohJ is essential for proper pollen tube tip growth. Plant Cell 26:1069–1080PubMedPubMedCentralCrossRefGoogle Scholar
  176. Keller T, Damude HG, Werner D, Doerner P, Dixon RA, Lamb C (1998) A plant homolog of the neutrophil NADPH Oxidase gp91 phox subunit gene encodes a plasma membrane protein with Ca2+ binding motifs. Plant Cell 10(2):255–266PubMedPubMedCentralGoogle Scholar
  177. Ketelaar T (2013) The actin cytoskeleton in root hairs: all is fine at the tip. Curr Opin Plant Biol 16:749–756PubMedCrossRefGoogle Scholar
  178. Ketelaar T, Faivre-moskalenko C, Esseling JJ, de Ruijter NC, Grierson CS, Dogterom M, Emons AM (2002) Positioning of nuclei in Arabidopsis root hairs: an actin-regulated process of tip growth. Plant Cell 14:2941–2955PubMedPubMedCentralCrossRefGoogle Scholar
  179. 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 15:285–292PubMedPubMedCentralCrossRefGoogle Scholar
  180. 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 14:145–149PubMedCrossRefGoogle Scholar
  181. 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 174:57–62PubMedCrossRefGoogle Scholar
  182. Khurana P, Henty JL, Huang S, Staiger AM, Blanchoin L, Staiger CJ (2010) Arabidopsis VILLIN1 and VILLIN3 have overlapping and distinct activities in actin bundle formation and turnover. Plant Cell 22:2727–2748PubMedPubMedCentralCrossRefGoogle Scholar
  183. Kiefer CS, Claes AR, Nzayisenga J-C, Pietra S, Stanislas T, Hüser A, Ikeda Y, Grebe M (2015) Arabidopsis AIP1-2 restricted by WER-mediated patterning modulates planar polarity. Development 142:151–161PubMedPubMedCentralCrossRefGoogle Scholar
  184. Kijima ST, Hirose K, Kong SG, Wada M, Uyeda TQ (2016) Distinct biochemical properties of Arabidopsis thaliana actin isoforms. Plant Cell Physiol 57:46–56PubMedCrossRefGoogle Scholar
  185. Kimura S, Kaya H, Kawarazaki T, Hiraoka G, Senzaki E, Michikawa M, Kuchitsu K (2012) Protein phosphorylation is a prerequisite for the Ca2+-dependent activation of Arabidopsis NADPH oxidases and may function as a trigger for the positive feedback regulation of Ca2+ and reactive oxygen species. Biochim Biophys Acta 1823:398–405PubMedCrossRefGoogle Scholar
  186. Klahre U, Chua NH (1999) The Arabidopsis ACTIN-RELATED PROTEIN 2 (AtARP2) promoter directs expression in xylem precursor cells and pollen. Plant Mol Biol 41:65–73PubMedCrossRefGoogle Scholar
  187. Klahre U, Kost B (2006) Tobacco RhoGTPase ACTIVATING PROTEIN1 spatially restricts signaling of RAC/Rop to the apex of pollen tubes. Plant Cell 18:3033–3046PubMedPubMedCentralCrossRefGoogle Scholar
  188. Klahre U, Becker C, Schmitt AC, Kost B (2006) Nt-RhoGDI2 regulates Rac/Rop signaling and polar cell growth in tobacco pollen tubes. Plant J 46:1018–1031PubMedCrossRefGoogle Scholar
  189. Kohler C, Neuhaus G (2000) Characterisation of calmodulin binding to cyclic nucleotide-gated ion channels from Arabidopsis thaliana. Febs Lett 471:133–136PubMedCrossRefGoogle Scholar
  190. Konrad KR, Wudick MM, Feijó JA (2011) Calcium regulation of tip growth: new genes for old mechanisms. Curr Opin Plant Biol 14:721–730PubMedCrossRefGoogle Scholar
  191. Kost B (2010) Regulatory and cellular functions of plant RhoGAPs and RhoGDIs. In: Yalovsky S et al (eds) Integrated G proteins signaling in plants. Springer, Berlin, pp 27–48CrossRefGoogle Scholar
  192. 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 145:317–330PubMedPubMedCentralCrossRefGoogle Scholar
  193. Kovar DR, Pollard TD (2004) Insertional assembly of actin filament barbed ends in association with formins produces piconewton forces. Proc Natl Acad Sci USA 101:14725–14730PubMedPubMedCentralCrossRefGoogle Scholar
  194. Kovar DR, Kuhn JR, Tichy AL, Pollard TD (2003) The fission yeast cytokinesis formin Cdc12p is a barbed end actin filament capping protein gated by profilin. J Cell Biol 161:875–887PubMedPubMedCentralCrossRefGoogle Scholar
  195. Kuhtreiber WM, Jaffe LF (1990) Detection of extracellular calcium gradients with a calcium-specific vibrating electrode. J Cell Biol 110:1565–1573PubMedCrossRefGoogle Scholar
  196. Kunz C, Chang A, Faure JD, Clarke AE, Polya GM, Anderson MA (1996) Phosphorylation of style S-RNases by Ca2+-dependent protein kinases from pollen tubes. Sex Plant Reprod 9:25–34CrossRefGoogle Scholar
  197. Kwak BH (1967) Studies on cellular site of calcium action in promoting pollen growth. Physiol Plant 20:825–833CrossRefGoogle Scholar
  198. Ladwig F, Dahlke RI, Stührwohldt N, Hartmann J, Harter K, Sauter M (2015) Phytosulfokine regulates growth in Arabidopsis through a response module at the plasma membrane that includes CYCLIC NUCLEOTIDE-GATED CHANNEL17, H+-ATPase, and BAK1. Plant Cell 27:1718–1729PubMedPubMedCentralCrossRefGoogle Scholar
  199. Landoni M, de Francesco A, Galbiati M, Tonelli C (2010) A loss-of-function mutation in Calmodulin2 gene affects pollen germination in Arabidopsis thaliana. Plant Mol Biol 74:235–247PubMedCrossRefGoogle Scholar
  200. Lassig R, Gutermuth T, Bey TD, Konrad KR, Romeis T (2014) Pollen tube NAD(P)H oxidases act as a speed control to dampen growth rate oscillations during polarized cell growth. Plant J 78:94–106PubMedCrossRefGoogle Scholar
  201. 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
  202. Le J, El-Assal SE-D, Basu D, Basu D, Saad ME, Szymanski DB (2003) Requirements for Arabidopsis ATARP2 and ATARP3 during epidermal development. Curr Biol 13:1341–1347PubMedCrossRefGoogle Scholar
  203. Lee YJ, Szumlanski A, Nielsen E, Yang Z (2008) Rho-GTPase-dependent filamentous actin dynamics coordinate vesicle targeting and exocytosis during tip growth. J Cell Biol 181:1155–1168PubMedPubMedCentralCrossRefGoogle Scholar
  204. Lemmon MA (2008) Membrane recognition by phospholipid-binding domains. Nat Rev Mol Cell Biol 9:99–111PubMedCrossRefGoogle Scholar
  205. Lemoine R, Bürkle L, Barker L, Sakr S, Kühn C, Regnacq M, Gaillard C, Delrot S, Frommer WB (1999) Identification of a pollen specific sucrose-transporter-like protein NtSUT3 from tobacco. FEBS Lett 454:325–330PubMedCrossRefGoogle Scholar
  206. Lew RR (1996) Pressure regulation of the electrical properties of growing Arabidopsis thaliana L. root hairs. Plant Physiol 112:1089–1100PubMedPubMedCentralCrossRefGoogle Scholar
  207. 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 11:1731–1742PubMedPubMedCentralGoogle Scholar
  208. Li S, Blanchoin L, Yang Z, Lord EM (2003) The putative Arabidopsis Arp2/3 complex controls leaf cell morphogenesis. Plant Physiol 132:2034–2044PubMedPubMedCentralCrossRefGoogle Scholar
  209. Li S, Gu Y, Yan A, Lord E, Yang ZB (2008) RIP1 (ROP interactive partner 1)/ICR1 marks pollen germination sites and may act in the ROP1 pathway in the control of polarized pollen growth. Mol Plant 1:1021–1035PubMedCrossRefGoogle Scholar
  210. Li Y, Shen Y, Cai C, Zhong C, Zhu L, Yuan M, Ren H (2010) The type II Arabidopsis formin14 interacts with microtubules and microfilaments to regulate cell division. Plant Cell 22:2710–2726PubMedPubMedCentralCrossRefGoogle Scholar
  211. Li LJ, Ren F, Gao XQ, Wei PC, Wang XC (2013) The reorganization of actin filaments is required for vacuolar fusion of guard cells during stomatal opening in Arabidopsis. Plant Cell Environ 36:484–497PubMedCrossRefGoogle Scholar
  212. Li X, Li JH, Wang W, Chen NZ, Ma TS, Xi YN, Zhang XL, Lin HF, Bai Y, Huang SJ, Chen YL (2014) ARP2/3 complex-mediated actin dynamics is required for hydrogen peroxide-induced stomatal closure in Arabidopsis. Plant, Cell Environ 37:1548–1560CrossRefGoogle Scholar
  213. Limonta M, Romanowsky S, Olivari C, Bonza MC, Luoni L, Rosenberg A, Harper JF, De Michelis MI (2014) ACA12 is a deregulated isoform of plasma membrane Ca2+-ATPase of Arabidopsis thaliana. Plant Mol Biol 84:387–397PubMedCrossRefGoogle Scholar
  214. Lin C, Choi HS, Cho HT (2011a) Root hair-specific expansin A7 is required for root hair elongation in Arabidopsis. Mol Cells 31:393–397PubMedPubMedCentralCrossRefGoogle Scholar
  215. Lin W-D, Liao Y-Y, Yang TJW, Pan CY, Buckhout TJ, Schmidt W (2011b) Coexpression-based clustering of Arabidopsis root genes predicts functional modules in early phosphate deficiency signaling. Plant Physiol 155:1383–1402PubMedPubMedCentralCrossRefGoogle Scholar
  216. Lin D, Nagawa S, Chen J, Cao L, Chen X, Xu T, Li H, Dhonukshe P, Yamamuro C, Friml J, Scheres B, Fu Y, Yang Z (2012) A ROP GTPase-dependent auxin signaling pathway regulates the subcellular distribution of PIN2 in Arabidopsis roots. Curr Biol 22:1319–1325PubMedPubMedCentralCrossRefGoogle Scholar
  217. Lin D, Cao L, Zhou Z, Zhu L, Ehrhardt D, Yang Z, Fu Y (2013) Rho GTPase signaling activates microtubule severing to promote microtubule ordering in Arabidopsis. Curr Biol 23:290–297PubMedCrossRefGoogle Scholar
  218. Liszkay A, Zalm E Van Der, Schopfer P (2004) Production of reactive oxygen intermediates (O2 •−, H2O2, and .OH) by maize roots and their role in wall loosening and elongation growth Plant Physiol 136:3114–3123Google Scholar
  219. Logan DC, Knight MR (2003) Mitochondrial and cytosolic calcium dynamics are differentially regulated in plants. Plant Physiol 133:21–24PubMedPubMedCentralCrossRefGoogle Scholar
  220. Lommel C, Felle HH (1997) Transport of Ca²+ across the tonoplast of intact vacuoles from Chenopodium album L. suspension cells : ATP-dependent import and inositol-1, 4, 5-trisphosphate-induced release. Planta 201(4):477–486CrossRefGoogle Scholar
  221. Loro G, Drago I, Pozzan T, Schiavo FL, Zottini M, Costa A (2012) Targeting of Cameleons to various subcellular compartments reveals a strict cytoplasmic/mitochondrial Ca2+ handling relationship in plant cells. Plant J 71:1–13PubMedCrossRefGoogle Scholar
  222. Lovy-Wheeler A, Kunkel JG, Allwood EG, Hussey PJ, Hepler PK (2006) Oscillatory increases in alkalinity anticipate growth and may regulate actin dynamics in pollen tubes of Lily. Plant Cell 18(9):2182–2193PubMedPubMedCentralCrossRefGoogle Scholar
  223. Lovy-Wheeler A, Cárdenas L, Kunkel JG, Hepler PK (2007) Differential organelle movement on the actin cytoskeleton in lily pollen tubes. Cell Motil Cytoskeleton 64:217–232PubMedCrossRefGoogle Scholar
  224. Lu Y, Chanroj S, Zulkifli L, Johnson MA, Uozumi N, Cheung A, Sze H (2011) Pollen tubes lacking a pair of K+ transporters fail to target ovules in Arabidopsis. Plant Cell 23:81–93PubMedPubMedCentralCrossRefGoogle Scholar
  225. Lucca N, León G (2012) Arabidopsis ACA7, encoding a putative auto-regulated Ca2+-ATPase, is required for normal pollen development. Plant Cell Rep 31:651–659PubMedCrossRefGoogle Scholar
  226. Maciver SK, Hussey PJ (2002) The ADF/cofilin family: actin-remodeling proteins. Genome Biol 3(5):reviews3007Google Scholar
  227. Madison SL, Buchanan ML, Glass JD, McClain TF, Park E, Nebenführ A (2015) Class XI myosins move specific organelles in pollen tubes and are required for normal fertility and pollen tube growth in Arabidopsis. Plant Physiol 169:1946–1960PubMedPubMedCentralGoogle Scholar
  228. Mähs A, Steinhorst L, Han JP, Shen LK, Wang Y, Kudla J (2013) The calcineurin B-like Ca2+ sensors CBL1 and CBL9 function in pollen germination and pollen tube growth in Arabidopsis. Mol Plant 6:1149–1162PubMedCrossRefGoogle Scholar
  229. Malhó R (1998) Role of 1,4,5-inositol triphosphate-induced Ca2+ release in pollen tube orientation. Sex Plant Reprod 11:231–235CrossRefGoogle Scholar
  230. Malhó R, Trewavas A (1996) localized apical increases of cytosolic free calcium control pollen tube orientation. Plant Cell 8:1935–1949PubMedPubMedCentralCrossRefGoogle Scholar
  231. Maris A, Suslov D, Fry SC, Verbelen JP, Vissenberg K (2009) Enzymic characterization of two recombinant xyloglucan endotransglucosylase/hydrolase (XTH) proteins of Arabidopsis and their effect on root growth and cell wall extension. J Exp Bot 60:3959–3972PubMedCrossRefGoogle Scholar
  232. Maris A, Kaewthai N, Eklöf JM, Miller JG, Brumer H, Fry SC, Verbelen JP, Vissenberg K (2011) Differences in enzymic properties of five recombinant xyloglucan endotransglucosylase/hydrolase (XTH) proteins of Arabidopsis thaliana. J Exp Bot 62:261–271PubMedCrossRefGoogle Scholar
  233. Maser P, Thomine S, Schroeder JI, Ward JM, Hirschi K, Sze H, Talke IN, Amtmann A, Maathuis FJ, Sanders D, Harper JF, Tchieu J, Gribskov M, Persans MW, Salt DE, Kim SA, Guerinot ML (2001) Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiol 126:1646–1667PubMedPubMedCentralCrossRefGoogle Scholar
  234. 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 126:5559–5568PubMedGoogle Scholar
  235. 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 15:1632–1645PubMedPubMedCentralCrossRefGoogle Scholar
  236. 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 130:3137–3146PubMedCrossRefGoogle Scholar
  237. McDowell JM, An YQ, Huang S, McKinney EC, Meagher RB (1996a) The Arabidopsis ACT7 actin gene is expressed in rapidly developing tissues and responds to several external stimuli. Plant Physiol 111:699–711PubMedPubMedCentralCrossRefGoogle Scholar
  238. McDowell JM, Huang S, Mckinney EC, An YQ, Meagher RB (1996b) Structure and evolution of the actin gene family in Arabidopsis thaliana. Genetics 142:587–602PubMedPubMedCentralGoogle Scholar
  239. McKinney EC, Meagher RB (1998) Members of the Arabidopsis actin gene family are widely dispersed in the genome. Genetics 149:663–675PubMedPubMedCentralGoogle Scholar
  240. McKinney EC, Kandasamy MK, Meagher RB (2001) Small changes in the regulation of one Arabidopsis profilin isovariant, PRF1, alter seedling development. Plant Cell 13:1179–1191PubMedPubMedCentralCrossRefGoogle Scholar
  241. McQueen-Mason SJ, Cosgrove DJ (1995) Expansin mode of action on cell walls. Plant Physiol 107:87–100PubMedPubMedCentralCrossRefGoogle Scholar
  242. McQueen-Mason S, Durachko DM, Cosgrove DJ (1992) Two endogenous proteins that induce cell wall extension in plants. Plant Cell 4:1425–1433PubMedPubMedCentralCrossRefGoogle Scholar
  243. Meharg A, Blatt M (1995) NO3- transport across the plasma membrane of Arabidopsis thaliana root hairs: kinetic control by pH and membrane voltage. J Membr Biol 145:49–66PubMedCrossRefGoogle Scholar
  244. Messerli MA, Danuser G, Robinson KR (1999) Pulsatile influxes of H+, K+ and Ca2+ lag growth pulses of Lilium longiflorum pollen tubes. J Cell Sci 112:1497–1509PubMedGoogle Scholar
  245. Messerli MA, Créton R, Jaffe LF, Robinson KR (2000) Periodic increases in elongation rate precede increases in cytosolic Ca2+ during pollen tube growth. Dev Biol 222:84–98PubMedCrossRefGoogle Scholar
  246. Michalak M, Groenendyk J, Gold LI, Opas M (2009) Calreticulin, a multi-process calcium-buffering chaperone of the endoplasmic reticulum. Biochem J 417:651–666PubMedCrossRefGoogle Scholar
  247. Michard E, Dias P, Feijó JA (2008) Tobacco pollen tubes as cellular models for ion dynamics: improved spatial and temporal resolution of extracellular flux and free cytosolic concentration of calcium and protons using pHluorin and YC3.1 CaMeleon. Sex Plant Reprod 21(3):169–181CrossRefGoogle Scholar
  248. Michard E, Alves F, Feijó JA (2009) The role of ion fluxes in polarized cell growth and morphogenesis: the pollen tube as an experimental paradigm. Int J Dev Biol 53:1609–1622PubMedCrossRefGoogle Scholar
  249. Michard E, Lima PT, Borges F, Silva AC, Portes MT, Carvalho JE, Gilliham M, Liu LH, Obermeyer G, Feijó JA (2011) Glutamate receptor-like genes form Ca2+ channels in pollen tubes and are regulated by pistil D-serine. Science 332:434–437PubMedCrossRefGoogle Scholar
  250. Michelli F (2001) Pectin methylesterases: cell wall enzymes with important roles in plant physiology. Trends Plant Sci 6:414–419CrossRefGoogle Scholar
  251. Michelot A, Guérin C, Huang S, Ingouff M, Richard S, Rodiuc N, Staiger CJ, Blanchoin L (2005) The formin homology 1 domain modulates the actin nucleation and bundling activity of Arabidopsis FORMIN1. Plant Cell 17:2296–2313PubMedPubMedCentralCrossRefGoogle Scholar
  252. Miedema H, Demidchik V, Véry AA, Bothwell JH, Brownlee C, Davies JM (2008) Two voltage-dependent calcium channels co-exist in the apical plasma membrane of Arabidopsis thaliana root hairs. New Phytol 179:378–385PubMedCrossRefGoogle Scholar
  253. 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 17:141–154CrossRefGoogle Scholar
  254. Mitchell KJ, Pinton P, Varadi A, Tacchetti C, Ainscow EK, Pozzan T, Rizzuto R, Rutter GA (2001) Dense core secretory vesicles revealed as a dynamic Ca2+ store in neuroendocrine cells with a vesicle-associated membrane protein aequorin chimaera. J Cell Biol 155:41–51PubMedPubMedCentralCrossRefGoogle Scholar
  255. Młodzińska E, Kłobus G, Christensen MD, Fuglsang AT (2015) The plasma membrane H+-ATPase AHA2 contributes to the root architecture in response to different nitrogen supply. Physiol Plant 154:270–282PubMedCrossRefGoogle Scholar
  256. 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 20:2779–2788PubMedPubMedCentralCrossRefGoogle Scholar
  257. 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 104:20996–21001PubMedPubMedCentralCrossRefGoogle Scholar
  258. 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 147:1690–1698PubMedPubMedCentralCrossRefGoogle Scholar
  259. Monshausen GB, Bibikova TN, Weisenseel MH, Gilroy S (2009) Ca2+ regulates reactive oxygen species production and pH during mechanosensing in Arabidopsis roots. Plant Cell 21:2341–2356PubMedPubMedCentralCrossRefGoogle Scholar
  260. Monteiro D, Liu Q, Lisboa S, Scherer GE, Quader H, Malhó R (2005) Phosphoinositides and phosphatidic acid regulate pollen tube growth and reorientation through modulation of [Ca2+]c and membrane secretion. J Exp Bot 56:1665–1674PubMedCrossRefGoogle Scholar
  261. Moriau L, Michelet B, Bogaerts P, Lambert L, Michel A, Oufattole M, Boutry M (1999) Expression analysis of two gene subfamilies encoding the plasma membrane H+-ATPase in Nicotiana plumbaginifolia reveals the major transport functions of this enzyme. Plant J 19:31–41PubMedCrossRefGoogle Scholar
  262. Mouline K, Véry A-A, Gaymard F, Boucherez J, Pilot G, Devic M, Bouchez D, Thibaud JB, Sentenac H (2002) Pollen tube development and competitive ability are impaired by disruption of a Shaker K+ channel in Arabidopsis. Genes Dev 16:339–350PubMedPubMedCentralCrossRefGoogle Scholar
  263. Moutinho A, Hussey PJ, Trewavas AJ, Malhó R (2001) cAMP acts as a second messenger in pollen tube growth and reorientation. Proc Natl Acad Sci USA 98:10481–10486PubMedPubMedCentralCrossRefGoogle Scholar
  264. Mucha E, Hoefle C, Hückelhoven R, Berken A (2010) RIP3 and AtKinesin-13A - a novel interaction linking Rho proteins of plants to microtubules. Eur J Cell Biol 89:906–916PubMedCrossRefGoogle Scholar
  265. Myers C, Romanowsky SM, Barron YD, Garg S, Azuse CL, Curran A, Davis RM, Hatton J, Harmon AC, Harper JF (2009) Calcium-dependent protein kinases regulate polarized tip growth in pollen tubes. Plant J 59:528–539PubMedCrossRefGoogle Scholar
  266. Nagawa S, Xu T, Yang Z (2010) RHO GTPase in plants: conservation and invention of regulators and effectors. Small GTPases 1:78–88PubMedPubMedCentralCrossRefGoogle Scholar
  267. Nakagawa Y, Katagiri T, Shinozaki K, Qi Z, Tatsumi H, Furuichi T, Kishigami A, Sokabe M, Kojima I, Sato S, Kato T, Tabata S, Iida K, Terashima A, Nakano M, Ikeda M, Yamanaka T, Iida H (2007) Arabidopsis plasma membrane protein crucial for Ca2+ influx and touch sensing in roots. Proc Natl Acad Sci USA 104:3639–3644PubMedPubMedCentralCrossRefGoogle Scholar
  268. Newcomb EH (1965) Cytoplasmic microtubule and wall microfibril orientation in root hairs of radish. J Cell Biol 27:575–589PubMedPubMedCentralCrossRefGoogle Scholar
  269. Nibau C, Cheung A (2011) New insights into the functional roles of CrRLKs in the control of plant cell growth and development. Plant Signal Behav 6:655–659PubMedPubMedCentralCrossRefGoogle Scholar
  270. Nibau C, Wu H ming, Cheung AY (2006) RAC/ROP GTPases: “hubs” for signal integration and diversification in plants. Trends Plant Sci 11:309–315Google Scholar
  271. Nishimura T, Yokota E, Wada T, Shimmen T, Okada K (2003) An Arabidopsis ACT2 dominant-negative mutation, which disturbs F-actin polymerization, reveals its distinctive function in root development. Plant Cell Physiol 44:1131–1140PubMedCrossRefGoogle Scholar
  272. Nishitani K, Vissenberg K (2007) Roles of the XTH protein family in the expanding cell. In: Verbelen JP, Vissenberg K (eds) The expanding cell. Plant cell monographs, vol 5. Springer, Berlin pp 89–116Google Scholar
  273. Nissen KS, Willats WGT, Malinovsky FG (2016) Understanding CrRLK1L function: cell walls and growth control. Trends Plant Sci 21(6):516–527PubMedCrossRefGoogle Scholar
  274. Nomura H, Shiina T (2014) Calcium signaling in plant endosymbiotic organelles: mechanism and role in physiology. Mol Plant 7:1094–1104PubMedCrossRefGoogle Scholar
  275. Obermeyer G, Weisenseel MH (1991) Calcium channel blocker and calmodulin antagonists affect the gradient of free calcium ions in lily pollen tubes. Eur J Cell Biol 56:319–327PubMedGoogle Scholar
  276. Ogasawara Y, Kaya H, Hiraoka G, Yumoto F, Kimura S, Kadota Y, Hishinuma H, Senzaki E, Yamagoe S, Nagata K, Nara M, Suzuki K, Tanokura M, Kuchitsu K (2008) Synergistic activation of the Arabidopsis NADPH oxidase AtrbohD by Ca2+ and phosphorylation. J Biol Chem 283:8885–8892PubMedCrossRefGoogle Scholar
  277. Oja V, Savchenko G, Jakob B, Heber U (1999) pH and buffer capacities of apoplastic and cytoplasmic cell compartments in leaves. Planta 209:239–249PubMedCrossRefGoogle Scholar
  278. Ojangu EL, Järve 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 230:193–202PubMedCrossRefGoogle Scholar
  279. Okada K, Ravi H, Smith EM, Goode BL (2006) AIP1 and Cofilin promote rapid turnover of yeast actin patches and cables: a coordinated mechanism for severing and capping filaments. Mol Biol Cell 17:2855–2868PubMedPubMedCentralCrossRefGoogle Scholar
  280. Ono S, Mohri K, Ono K (2004) Microscopic evidence that Actin-interacting Protein 1 actively disassembles actin-depolymerizing factor/cofilin-bound actin filaments. J Biol Chem 279:14207–14212PubMedCrossRefGoogle Scholar
  281. Palmgren MG (2001) Plant plasma membrane H+-atpases. Annu Rev Plant Physiol Plant Mol Biol 52:817–845PubMedCrossRefGoogle Scholar
  282. Pang CY, Wang H, Pang Y, Xu C, Jiao Y, Qin YM, Western TL, Yu SX, Zhu YX (2010) Comparative proteomics indicates that biosynthesis of pectic precursors is important for cotton fiber and Arabidopsis root hair elongation. Mol Cell Proteomics 9:2019–2033PubMedPubMedCentralCrossRefGoogle Scholar
  283. Park YB, Cosgrove DJ (2012) changes in cell wall biomechanical properties in the xyloglucan-deficient xxt1/xxt2 mutant of Arabidopsis. Plant Physiol 158:465–475PubMedCrossRefGoogle Scholar
  284. Park E, Nebenführ A (2013) Myosin XIK of Arabidopsis thaliana accumulates at the root hair tip and is required for fast root hair growth. PLoS One 8:e76745PubMedPubMedCentralCrossRefGoogle Scholar
  285. Park S, Szumlanski AL, Gu F, Guo F, Nielsen E (2011) A role for CSLD3 during cell-wall synthesis in apical plasma membranes of tip-growing root-hair cells. Nat Cell Biol 13:973–980PubMedCrossRefGoogle Scholar
  286. Pei ZM, Murata Y, Benning G, Thomine S, Klüsener B, Allen GJ, Grill E, Schroeder JI (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406:731–734PubMedCrossRefGoogle Scholar
  287. Pei W, Du F, Zhang Y, He T, Ren H (2012) Control of the actin cytoskeleton in root hair development. Plant Sci 187:10–18PubMedCrossRefGoogle Scholar
  288. Pena MJ, Kong Y, York WS, O’Neill MA (2012) A galacturonic acid-containing xyloglucan is involved in Arabidopsis root hair tip growth. Plant Cell 24:4511–4524PubMedPubMedCentralCrossRefGoogle Scholar
  289. Peremyslov VV, Prokhnevsky AL, Avisar D, Dolja VV (2008) Two class XI myosins function in organelle trafficking and root hair development in Arabidopsis. Plant Physiol 146:1109–1116PubMedPubMedCentralCrossRefGoogle Scholar
  290. Peremyslov VV, Prokhnevsky AL, Dolja VV (2010) Class XI myosins are required for development, cell expansion, and F-Actin organization in Arabidopsis. Plant Cell 22:1883–1897PubMedPubMedCentralCrossRefGoogle Scholar
  291. Peremyslov VV, Klocko AL, Fowler JE, Dolja VV (2012) Arabidopsis Myosin XI-K Localizes to the Motile Endomembrane Vesicles Associated with F-actin. Front Plant Sci 3:1–10CrossRefGoogle Scholar
  292. Peremyslov VV, Morgun EA, Kurth EG, Makarova KS, Koonin EV, Dolja VV (2013) Identification of myosin XI receptors in Arabidopsis defines a distinct class of transport vesicles. Plant Cell 25:3022–3038PubMedPubMedCentralCrossRefGoogle Scholar
  293. Pertl H, Himly M, Gehwolf R, Kriechbaumer R, Strasser D, Michalke W, Richter K, Ferreira F, Obermeyer G (2001) Molecular and physiological characterisation of a 14-3-3 protein from lily pollen grains regulating the activity of the plasma membrane H+-ATPase during pollen grain germination and tube growth. Planta 213:132–141PubMedCrossRefGoogle Scholar
  294. Petersen J, Nielsen O, Egel R, Hagan IM (1998) FH3, a domain found in formins, targets the fission yeast formin Fus1 to the projection tip during conjugation. J Cell Biol 141:1217–1228PubMedPubMedCentralCrossRefGoogle Scholar
  295. Pierson ES, Miller DD, Callaham DA, van Aken J, Hackett G, Hepler PK (1996) Tip-localized calcium entry fluctuates during pollen tube growth. Dev Biol 174:160–173PubMedCrossRefGoogle Scholar
  296. Pina C, Pinto F, Feijó JA, Becker JD (2005) Gene family analysis of the Arabidopsis pollen transcriptome reveals biological implications for cell growth, division control, and gene expression regulation. Plant Physiol 138:744–756PubMedPubMedCentralCrossRefGoogle Scholar
  297. Plieth C, Hansen UP (1998) Cytosolic Ca2+ and H+ buffers in green algae: a reply. Protoplasma 203:210–213CrossRefGoogle Scholar
  298. Plieth C, Trewavas AJ (2002) Reorientation of seedlings in the earth’s gravitational field induces cytosolic calcium transients 1. Plant Physiol 129:786–796PubMedPubMedCentralCrossRefGoogle Scholar
  299. Plieth C, Sattelmacher B, Hansen UP (1997) Cytoplasmic Ca2+-H+-exchange buffers in green algae. Protoplasma 198:107–124CrossRefGoogle Scholar
  300. Pollard TD, Borisy GG (2003) Cellular motility driven by assembly and disassembly of actin filaments. Cell 112:453–465PubMedCrossRefGoogle Scholar
  301. Potocký M, Jones MA, Bezvoda R, Smirnoff N, Zárský V (2007) Reactive oxygen species produced by NADPH oxidase are involved in pollen tube growth. New Phytol 174:742–751PubMedCrossRefGoogle Scholar
  302. Poulter NS, Vatovec S, Franklin-Tong VE (2008) Microtubules are a target for self-incompatibility signaling in Papaver pollen. Plant Physiol 146:1358–1367PubMedPubMedCentralCrossRefGoogle Scholar
  303. 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 172:991–998PubMedPubMedCentralCrossRefGoogle Scholar
  304. Putney JW, Broad LM, Braun FJ, Lievremont JP, Bird GS (2001) Mechanisms of capacitative calcium entry. J Cell Sci 114:2223–2229PubMedGoogle Scholar
  305. Qin Y, Leydon AR, Manziello A, Pandey R, Mount D, Denic S, Vasic B, Johnson MA, Palanivelu R (2009) Penetration of the stigma and style elicits a novel transcriptome in pollen tubes, pointing to genes critical for growth in a pistil. PLoS Genet 5:e1000621PubMedPubMedCentralCrossRefGoogle Scholar
  306. Qu HY, Shang ZL, Zhang SL, Liu LM, Wu JY (2007) Identification of hyperpolarization-activated calcium channels in apical pollen tubes of Pyrus pyrifolia. New Phytol 174:524–536PubMedCrossRefGoogle Scholar
  307. Qu X, Zhang H, Xie Y, Wang J, Chen N, Huang S (2013) Arabidopsis villins promote actin turnover at pollen tube tips and facilitate the construction of actin collars. Plant Cell 25:1803–1817PubMedPubMedCentralCrossRefGoogle Scholar
  308. Ragel P, Ródenas R, García-Martín E, Andrés Z, Villalta I, Nieves-Cordones M, Rivero RM, Martínez V, Pardo JM, Quintero FJ, Rubio F (2015) CIPK23 regulates HAK5-mediated high-affinity K+ uptake in Arabidopsis roots. Plant Physiol 169:2863–2873PubMedPubMedCentralGoogle Scholar
  309. Rato C, Monteiro D, Hepler PK, Malhó R (2004) Calmodulin activity and cAMP signalling modulate growth and apical secretion in pollen tubes. Plant J 38:887–897PubMedCrossRefGoogle Scholar
  310. Rayle DL, Cleland RE (1992) The acid growth theory of auxin-induced cell elongation is alive and well. Plant Physiol 99:1271–1274PubMedPubMedCentralCrossRefGoogle Scholar
  311. Reguera M, Bassil E, Tajima H, Wimmer M, Chanoca A, Otegui MS, Paris N, Blumwald E (2015) pH regulation by NHX-Type antiporters is required for receptor-mediated protein trafficking to the vacuole in Arabidopsis. Plant Cell 27:1200–1217PubMedPubMedCentralCrossRefGoogle Scholar
  312. Reintanz B, Szyroki A, Ivashikina N, Ache P, Godde M, Becker D, Palme K, Hedrich R (2002) AtKC1, a silent Arabidopsis potassium channel alpha-subunit modulates root hair K+ influx. Proc Natl Acad Sci USA 99:4079–4084PubMedPubMedCentralCrossRefGoogle Scholar
  313. Reisen D, Hanson MR (2007) Association of six YFP-myosin XI-tail fusions with mobile plant cell organelles. BMC Plant Biol 7:6PubMedPubMedCentralCrossRefGoogle Scholar
  314. Rentel MC, Lecourieux D, Ouaked F, Usher SL (2004) OXI1 kinase is necessary for oxidative burst-mediated signalling in Arabidopsis. Nature 427:858–861PubMedCrossRefGoogle Scholar
  315. Richmond TA, Somerville CR (2001) Integrative approaches to determining Csl function. Plant Mol Biol 47:131–143PubMedCrossRefGoogle Scholar
  316. Rigas S, Debrosses G, Haralampidis K, Vicente-Agullo F, Feldmann KA, Grabov A, Dolan L, Hatzopoulos P (2001) TRH1 encodes a potassium transporter required for tip growth in Arabidopsis root hairs. Plant Cell 13:139–151PubMedPubMedCentralCrossRefGoogle Scholar
  317. Ringli C (2010) The hydroxyproline-rich glycoprotein domain of the Arabidopsis LRX1 requires Tyr for function but not for insolubilization in the cell wall. Plant J 63:662–669PubMedCrossRefGoogle Scholar
  318. 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 129:1464–1472PubMedPubMedCentralCrossRefGoogle Scholar
  319. Rocha AG, Vothknecht UC (2012) The role of calcium in chloroplasts-an intriguing and unresolved puzzle. Protoplasma 249:957–966PubMedCrossRefGoogle Scholar
  320. Rodriguez-Rosales M, Roldan M, Belver A, Donaire J (1989) Correlation between in-vitro germination capacity and proton extrusion in olive pollen. Plant Physiol Biochem 27:723–728Google Scholar
  321. Romero S, Le Clainche C, Didry D, Egile C, Pantaloni D, Carlier MF (2004) Formin is a processive motor that requires profilin to accelerate actin assembly and associated ATP hydrolysis. Cell 119:419–429PubMedCrossRefGoogle Scholar
  322. Rounds CM, Bezanilla M (2013) Growth mechanisms in tip-growing plant cells. Annu Rev Plant Biol 64:243–265PubMedCrossRefGoogle Scholar
  323. Rounds CM, Lubeck E, Hepler PK, Winship LJ (2011) Propidium iodide competes with Ca2+ to label pectin in pollen tubes and Arabidopsis root hairs. Plant Physiol 157:175–187PubMedPubMedCentralCrossRefGoogle Scholar
  324. Ruiz-Cristin J, Briskin D (1991) Characterization of a H+/NO3- symport associated with plasma membrane vesicles of maize roots using 36ClO3 as a radiotracer analog. Arch Biochem Biophys 285:74–82PubMedCrossRefGoogle Scholar
  325. Ruzicka DR, Kandasamy MK, McKinney EC, Burgos-Rivera B, Meagher RB (2007) The ancient subclasses of Arabidopsis Actin Depolymerizing Factor genes exhibit novel and differential expression. Plant J 52:460–472PubMedCrossRefGoogle Scholar
  326. 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 126:1281–1290PubMedPubMedCentralCrossRefGoogle Scholar
  327. Sakai T, Honing H Van Der, 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 53:157–171Google Scholar
  328. Šamaj J, Ovecka M, Hlavacka A, Lecourieux F, Meskiene I, Lichtscheidl I, Lenart P, Salaj J, Volkmann D, Bögre L, Baluska F, Hirt H (2002) Involvement of the mitogen-activated protein kinase SIMK in regulation of root hair tip growth. EMBO J 21:3296–3306PubMedPubMedCentralCrossRefGoogle Scholar
  329. Sanders D, Pelloux J, Brownlee C, Harper JF (2002) Calcium at the crossroads of signaling. Plant Cell 14(Suppl):S401–S417PubMedPubMedCentralGoogle Scholar
  330. Santi S, Schmidt W (2009) Dissecting iron deficiency-induced proton extrusion in Arabidopsis roots. New Phytol 183:1072–1084PubMedCrossRefGoogle Scholar
  331. Scheible WR, Pauly M (2004) Glycosyltransferases and cell wall biosynthesis: novel players and insights. Curr Opin Plant Biol 7:285–295PubMedCrossRefGoogle Scholar
  332. Schiefelbein JW, Shipley A, Rowse P (1992) Calcium influx at the tip of growing root hair cells of Arabidopsis thaliana. Planta 197:455–459Google Scholar
  333. 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 103:979–985PubMedPubMedCentralCrossRefGoogle Scholar
  334. Schiott M, Romanowsky SM, Baekgaard L, Jakobsen MK, Palmgren MG, Harper JF (2004) A plant plasma membrane Ca2+ pump is required for normal pollen tube growth and fertilization. Proc Natl Acad Sci USA 101:9502–9507PubMedPubMedCentralCrossRefGoogle Scholar
  335. Scholz-Starke J, Büttner M, Sauer N (2003) AtSTP6, a new pollen-specific H+-monosaccharide symporter from Arabidopsis. Plant Physiol 131:70–77PubMedPubMedCentralCrossRefGoogle Scholar
  336. Schönknecht G (2013) Calcium signals from the vacuole. Plants 2:589–614PubMedPubMedCentralCrossRefGoogle Scholar
  337. Schopfer P (1996) Hydrogen peroxide-mediated cell-wall stiffening in vitro in maize coleoptiles. Planta 199:43–49CrossRefGoogle Scholar
  338. Schopfer P (2001) Hydroxyl radical-induced cell-wall loosening in vitro and in vivo: implications for the control of elongation growth. Plant J 28:679–688PubMedCrossRefGoogle Scholar
  339. Shang ZL, Ma LG, Zhang HL, He RR, Wang XC, Cui SJ, Sun DY (2005) Ca2+ influx into lily pollen grains through a hyperpolarization-activated Ca2+-permeable channel which can be regulated by extracellular CaM. Plant Cell Physiol 46:598–608PubMedCrossRefGoogle Scholar
  340. Shimmen T, Hamatani M, Saito S, Yokota E, Mimura T, Fusetani N, Karaki H (1995) Roles of actin filaments in cytoplasmic streaming and organization of transvacuolar strands in root hair cells of Hydrocharis. Protoplasma 185:188–193CrossRefGoogle Scholar
  341. Shin DH, Cho MH, Kim TL, Yoo J, Kim JI, Han YJ, Song PS, Jeon JS, Bhoo SH, Hahn TR (2010) A small GTPase activator protein interacts with cytoplasmic phytochromes in regulating root development. J Biol Chem 285:32151–32159PubMedPubMedCentralCrossRefGoogle Scholar
  342. Sieberer BJ, Timmers ACJ, Lhuissier FGP, Emons AMC (2002) Endoplasmic microtubules configure the subapical cytoplasm and are required for fast growth of Medicago truncatula root hairs. Plant Physiol 130:977–988PubMedPubMedCentralCrossRefGoogle Scholar
  343. Simon M, Bruex A, Kainkaryam RM, Zheng X, Huang L, Woolf PJ, Schiefelbein J (2013) Tissue-specific profiling reveals transcriptome alterations in Arabidopsis mutants lacking morphological phenotypes. Plant Cell 25:3175–3185PubMedPubMedCentralCrossRefGoogle Scholar
  344. 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 14:187–193PubMedCrossRefGoogle Scholar
  345. Somerville C, Bauer S, Brininstool G, Facette M, Hamann T, Milne J, Osborne E, Paredez A, Persson S, Raab T, Vorwerk S, Youngs H (2004) Toward a systems approach to understanding plant cell walls. Sci 306:2206–2211CrossRefGoogle Scholar
  346. Song L-F, Zou J-J, Zhang WZ, Wu WH, Wang Y (2009) Ion transporters involved in pollen germination and pollen tube tip-growth. Plant Signal Behav 4:1193–1195PubMedPubMedCentralCrossRefGoogle Scholar
  347. Steinhorst L, Kudla J (2014) Signaling in cells and organisms - calcium holds the line. Curr Opin Plant Biol 22C:14–21CrossRefGoogle Scholar
  348. Steinhorst L, Mähs A, Ischebeck T, Zhang C, Zhang X, Arendt S, Schültke S, Heilmann I, Kudla J (2015) Vacuolar CBL-CIPK12 Ca2+-sensor-kinase complexes are required for polarized pollen tube growth. Curr Biol 25:1475–1482PubMedCrossRefGoogle Scholar
  349. Sun W, Li S, Xu J, Liu T, Shang Z (2009) H+-ATPase in the plasma membrane of Arabidopsis pollen cells is involved in extracellular calmodulin-promoted pollen germination. Prog Nat Sci 19:1071–1078CrossRefGoogle Scholar
  350. Sweeney HL, Houdusse A (2010) Structural and functional insights into the myosin motor mechanisms. Annu Rev Biophys 39:539–557PubMedCrossRefGoogle Scholar
  351. Sze H, Li X, Palmgren M (1999) Energization of plant cell membranes by H+-pumping ATPases. Regulation and biosynthesis. Plant Cell 11:677–690PubMedPubMedCentralGoogle Scholar
  352. Sze H, Frietsch S, Li X, Bock KW, Harper JF (2006) Genomic and molecular analyses of transporters in the male gametophyte. In: Plant cell monographs, vol 3. Springer, Berlin, pp 71–93Google Scholar
  353. 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 319:1241–1244PubMedCrossRefGoogle Scholar
  354. Talke IN, Blaudez D, Maathuis FJM, Sanders D (2003) CNGCs: prime targets of plant cyclic nucleotide signalling? Trends Plant Sci 8:286–293PubMedCrossRefGoogle Scholar
  355. Tao LZ, Cheung AY, Wu HM (2002) Plant Rac-like GTPases are activated by auxin and mediate auxin-responsive gene expression. Plant Cell 14:2745–2760PubMedPubMedCentralCrossRefGoogle Scholar
  356. Thion L, Mazars C, Thuleau P, Graziana A, Rossignol M, Moreau M, Ranjeva R (1996) Activation of plasma membrane voltage-dependent calcium-permeable channels by disruption of microtubules in carrot cells. FEBS Lett 393:13–18PubMedCrossRefGoogle Scholar
  357. 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 thaliana protoplasts, display constitutively large activities and a longer half-life in ton 2 mutant cells affected in the organization of cortical microtubules. Plant J 13:603–610PubMedCrossRefGoogle Scholar
  358. Tholl S, Moreau F, Hoffmann C, Arumugam K, Dieterle M, Moes D, Neumann K, Steinmetz A, Thomas C (2011) Arabidopsis actin-depolymerizing factors (ADFs) 1 and 9 display antagonist activities. FEBS Lett 585:1821–1827PubMedCrossRefGoogle Scholar
  359. Thomas MV (1982) Techniques in calcium research. Academic Press, New YorkGoogle Scholar
  360. Tian GW, Chen MH, Zaltsman A, Citovsky V (2006) Pollen-specific pectin methylesterase involved in pollen tube growth. Dev Biol 294:83–91PubMedCrossRefGoogle Scholar
  361. Timmers ACJ, Vallotton P, Heym C, Menzel D (2007) Microtubule dynamics in root hairs of Medicago truncatula. Eur J Cell Biol 86:69–83PubMedCrossRefGoogle Scholar
  362. 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
  363. Tominaga M, Kojima H, Yokota E, Nakamori R, Anson M, Shimmen T, Oiwa K (2012) Calcium-induced mechanical change in the neck domain alters the activity of plant myosin XI. J Biol Chem 287:30711–30718PubMedPubMedCentralCrossRefGoogle Scholar
  364. Torres MA, Dangl JL (2005) Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development. Curr Opin Plant Biol 8:397–403PubMedCrossRefGoogle Scholar
  365. Torres MA, Onouchi H, Hamada S, Machida C, Hammond-Kosack KE, Jones JD (1998) Six Arabidopsis thaliana homologues of the human respiratory burst oxidase (gp91(phox)). Plant J 14:365–370PubMedCrossRefGoogle Scholar
  366. Toyota M, Furuichi T, Tatsumi H, Sokabe M (2007) Cytoplasmic calcium increases in response to changes in the gravity vector in hypocotyls and petioles of Arabidopsis seedlings. Plant Physiol 146:505–514PubMedCrossRefGoogle Scholar
  367. Trewavas A (1999) Le calcium, c’est la vie: calcium makes waves. Plant Physiol 120:1–6PubMedPubMedCentralCrossRefGoogle Scholar
  368. Trewavas AJ, Malho R (1997) Signal perception and transduction: the origin of the phenotype. Plant Cell 9:1181–1195PubMedPubMedCentralCrossRefGoogle Scholar
  369. Tunc-Ozdemir M, Tang C, Ishka MR, Brown E, Groves NR, Myers CT, Rato C, Poulsen LR, McDowell S, Miller G, Mittler R, Harper JF (2013) A cyclic nucleotide-gated channel (CNGC16) in pollen is critical for stress tolerance in pollen reproductive development. Plant Physiol 161:1010–1020PubMedCrossRefGoogle Scholar
  370. Valenta R, Ferreira F, Grote M, Swoboda I, Vrtala S, Duchêne M, Deviller P, Meagher RB, McKinney E, Heberle-Bors E (1993) Identification of profilin as an actin-binding protein in higher plants. J Biol Chem 268:22777–22781PubMedGoogle Scholar
  371. Van Bruaene N, Joss G, Van Oostveldt P (2004) Reorganization and in vivo dynamics of microtubules during Arabidopsis root hair development. Plant Physiol 136:3905–3919PubMedPubMedCentralCrossRefGoogle Scholar
  372. van Gisbergen PAC, Bezanilla M (2013) Plant formins: membrane anchors for actin polymerization. Trends Cell Biol 23:227–233PubMedCrossRefGoogle Scholar
  373. Van Sandt VST, Suslov D, Verbelen JP, Vissenberg K (2007) Xyloglucan endotransglucosylase activity loosens a plant cell wall. Ann Bot 100:1467–1473PubMedPubMedCentralCrossRefGoogle Scholar
  374. Vassileva VN, Fujii Y, Ridge RW (2005) Microtubule dynamics in plants. Plant Biotechnol 22:171–178CrossRefGoogle Scholar
  375. Vazquez LA, Sanchez R, Hernandez-Barrera A, Zepeda-Jazo I, Sánchez F, Quinto C, Torres LC (2014) Actin polymerization drives polar growth in Arabidopsis root hair cells. Plant Signal Behav 9:e29401PubMedCentralCrossRefGoogle Scholar
  376. Velasquez SM, Ricardi MM, Dorosz JG, Fernandez PV, Nadra AD, Pol-Fachin L, Egelund J, Gille S, Harholt J, Ciancia M, Verli H, Pauly M, Bacic A, Olsen CE, Ulvskov P, Petersen BL, Somerville C, Iusem ND, Estevez JM (2011) O-glycosylated cell wall proteins are essential in root hair growth. Science 332:1401–1403PubMedCrossRefGoogle Scholar
  377. Véry AA, Davies JM (2000) Hyperpolarization-activated calcium channels at the tip of Arabidopsis root hairs. Proc Natl Acad Sci USA 97:9801–9806PubMedPubMedCentralCrossRefGoogle Scholar
  378. Veshaguri S, Christensen SM, Kemmer GC, Ghale G, Møller MP, Lohr C, Christensen AL, Justesen BH, Jørgensen IL, Schiller J, Hatzakis NS, Grabe M, Pomorski TG, Stamou D (2016) Direct observation of proton pumping by a eukaryotic P-type ATPase. Science 351:1469–1473PubMedPubMedCentralCrossRefGoogle Scholar
  379. Vidali L, Hepler P (1997) Characterization and localization of profiling in pollen grains and tubes of Lilium longiflorum. Cell Motil Cytoskeleton 36(4):323–338PubMedCrossRefGoogle Scholar
  380. Vidali L, van Gisbergen P a C, Guérin C, Franco P, Li M, Burkart GM, Augustine RC, Blanchoin L, Bezanilla M (2009) Rapid formin-mediated actin-filament elongation is essential for polarized plant cell growth. Proc Natl Acad Sci USA 106:13341–13346Google Scholar
  381. Vincill ED, Bieck AM, Spalding EP (2012) Ca2+ conduction by an amino acid-gated ion channel related to glutamate receptors. Plant Physiol 159:40–46PubMedPubMedCentralCrossRefGoogle Scholar
  382. Vissenberg K, Martinez-Vilchez IM, Verbelen JP, Miller JG, Fry SC (2000) In vivo colocalization of xyloglucan endotransglycosylase activity and its donor substrate in the elongation zone of Arabidopsis roots. Plant Cell 12:1229–1237PubMedPubMedCentralCrossRefGoogle Scholar
  383. 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 127:1125–1135PubMedPubMedCentralCrossRefGoogle Scholar
  384. Vissenberg K, Van Sandt V, Fry SC, Verbelen JP (2003) Xyloglucan endotransglucosylase action is high in the root elongation zone and in the trichoblasts of all vascular plants from Selaginella to Zea mays. J Exp Bot 54:335–344PubMedCrossRefGoogle Scholar
  385. Wagner S, Behera S, De Bortoli S, Logan DC, Fuchs P, Carraretto L, Teardo E, Cendron L, Nietzel T, Füßl M, Doccula FG, Navazio L, Fricker MD, Van Aken O, Finkemeier I, Meyer AJ, Szabò I, Costa A, Schwarzländer M (2015) The EF-hand Ca2+ binding protein MICU choreographs mitochondrial Ca2+ dynamics in Arabidopsis. Plant Cell 27:3190–3212PubMedPubMedCentralCrossRefGoogle Scholar
  386. Walter N, Holweg CL (2008) Head-neck domain of Arabidopsis myosin XI, MYA2, fused with GFP produces F-actin patterns that coincide with fast organelle streaming in different plant cells. BMC Plant Biol 8:74PubMedPubMedCentralCrossRefGoogle Scholar
  387. Wang X, Cnops G, Vanderhaeghen R, De Block S, Van Montagu M, Van Lijsebettens M (2001) AtCSLD3, a cellulose synthase-like gene important for root hair growth in Arabidopsis. Plant Physiol 126:575–586PubMedPubMedCentralCrossRefGoogle Scholar
  388. Wang Y, Zhang WZ, Song LF, Zou JJ, Su Z, Wu WH (2008) Transcriptome analyses show changes in gene expression to accompany pollen germination and tube growth in Arabidopsis. Plant Physiol 148:1201–1211PubMedPubMedCentralCrossRefGoogle Scholar
  389. Wang J, Zhang Y, Wu J, Meng L, Ren H (2013) At FH16, an Arabidopsis type II formin, binds and bundles both microfilaments and microtubules, and preferentially binds to microtubules. J Integr Plant Biol 55:1002–1015PubMedCrossRefGoogle Scholar
  390. Wang SS, Diao WZ, Yang X, Qiao Z, Wang M, Acharya BR, Zhang W (2015a) Arabidopsis thaliana CML25 mediates the Ca2+ regulation of K + transmembrane trafficking during pollen germination and tube elongation. Plant Cell Environ 38:2372–2386PubMedCrossRefGoogle Scholar
  391. Wang Y, Dindas J, Rienmüller F, Krebs M, Waadt R, Schumacher K, Wu WH, Hedrich R, Roelfsema MR (2015b) Cytosolic Ca2+ signals enhance the vacuolar ion conductivity of bulging Arabidopsis root hair cells. Mol Plant 8:1665–1674PubMedCrossRefGoogle Scholar
  392. Wang XP, Chen LM, Liu WX, Shen LK, Wang FL, Zhou Y, Zhang Z, Wu WH, Wang Y (2016) AtKC1 and CIPK23 synergistically modulate AKT1-mediated low potassium stress responses in Arabidopsis. Plant Physiol 170:2264–2277PubMedPubMedCentralCrossRefGoogle Scholar
  393. Ward JM, Mäser P, Schroeder JI (2009) Plant ion channels: gene families, physiology, and functional genomics analyses. Annu Rev Physiol 71:59–82PubMedPubMedCentralCrossRefGoogle Scholar
  394. Watanabe N, Madaule P, Reid T, Ishizaki T, Watanabe G, Kakizuka A, Saito Y, Nakao K, Jockusch BM, Narumiya S (1997) p140mDia, a mammalian homolog of Drosophila diaphanous, is a target protein for Rho small GTPase and is a ligand for profilin. EMBO J 16:3044–3056PubMedPubMedCentralCrossRefGoogle Scholar
  395. Weerasinghe R, Collings D, Johannes E, Allen N (2003) The distributional changes and role of microtubules in Nod factor-challenged Medicago sativa root hairs. Planta 218:276–287PubMedCrossRefGoogle Scholar
  396. 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 411:610–613PubMedCrossRefGoogle Scholar
  397. Williamson RE, Burn JE, Birch R, Baskin TI, Arioli T, Betzner AS, Cork A (2001) Morphology of rsw1, a cellulose-deficient mutant of Arabidopsis thaliana. Protoplasma 215:116–127PubMedCrossRefGoogle Scholar
  398. Winter D, Vinegar B, Nahal H, Ammar R, Wilson GV, Provart NJ (2007) An “electronic fluorescent pictograph” browser for exploring and analyzing large-scale biological data sets. PLoS One 2:e718PubMedPubMedCentralCrossRefGoogle Scholar
  399. Wolf S, Höfte H (2014) Growth control: a saga of cell walls, ros, and peptide receptors. Plant Cell 26:1848–1856PubMedPubMedCentralCrossRefGoogle Scholar
  400. Wolf S, Hématy K, Höfte H (2012) Growth control and cell wall signaling in plants. Annu Rev Plant Biol 63:381–407PubMedCrossRefGoogle Scholar
  401. Won SK, Lee YJ, Lee HY, Heo YK, Cho M, Cho HT (2009) Cis-element- and transcriptome-based screening of root hair-specific genes and their functional characterization in Arabidopsis. Plant Physiol 150:1459–1473PubMedPubMedCentralCrossRefGoogle Scholar
  402. Wu G, Li H, Yang Z (2000) Arabidopsis RopGAPs are a novel family of Rho GTPase-activating proteins that require the Cdc42/Rac-interactive binding motif for Rop-specific GTPase stimulation. Plant Physiol 124:1625–1636PubMedPubMedCentralCrossRefGoogle Scholar
  403. Wu G, Gu Y, Li S, Yang Z (2001) A genome-wide analysis of Arabidopsis Rop-interactive CRIB motif-containing proteins that act as Rop GTPase targets. Plant Cell 13:2841–2856PubMedPubMedCentralCrossRefGoogle Scholar
  404. Wu Y, Xu X, Li S, Liu T, Ma L, Shang Z (2007) Heterotrimeric G-protein participation in Arabidopsis pollen germination through modulation of a plasmamembrane hyperpolarization-activated Ca 2+-permeable channel. New Phytol 176:550–559PubMedCrossRefGoogle Scholar
  405. Wu J, Shang Z, Wu J, Jiang X, Moschou PN, Sun W, Roubelakis-Angelakis KA, Zhang S (2010) Spermidine oxidase-derived H2O2 regulates pollen plasma membrane hyperpolarization-activated Ca2+-permeable channels and pollen tube growth. Plant J 63:1042–1053PubMedCrossRefGoogle Scholar
  406. Wu J, Qu H, Jin C, Shang Z, Wu J, Xu G, Gao Y, Zhang S (2011) cAMP activates hyperpolarization-activated Ca2+ channels in the pollen of Pyrus pyrifolia. Plant Cell Rep 30:1193–1200PubMedCrossRefGoogle Scholar
  407. Wu Y, Zhao S, Tian H, He Y, Xiong W, Guo L, Wu Y (2013) CPK3-phosphorylated RhoGDI1 is essential in the development of Arabidopsis seedlings and leaf epidermal cells. J Exp Bot 64:3327–3338PubMedPubMedCentralCrossRefGoogle Scholar
  408. Wudick MM, Feijó JA (2014) At the intersection: merging Ca2+ and ROS signalling pathways in pollen. Mol Plant 7:1595–1597PubMedCrossRefGoogle Scholar
  409. Wymer C, Bibikova T, Gilroy S (1997) Cytoplasmic free calcium distributions during the development of root hairs of Arabidopsis thaliana. Plant J 12:427–439PubMedCrossRefGoogle Scholar
  410. Yalovsky S, Bloch D, Sorek N, Kost B (2008) Regulation of membrane trafficking, cytoskeleton dynamics, and cell polarity by ROP/RAC GTPases. Plant Physiol 147:1527–1543PubMedPubMedCentralCrossRefGoogle Scholar
  411. Yamanaka T, Nakagawa Y, Mori K, Nakano M, Imamura T, Kataoka H, Terashima A, Iida K, Kojima I, Katagiri T, Shinozaki K, Iida H (2010) MCA1 and MCA2 that mediate Ca2+ uptake have distinct and overlapping roles in Arabidopsis. Plant Physiol 152:1284–1296PubMedPubMedCentralCrossRefGoogle Scholar
  412. Yan A, Xu G, Yang ZB (2009) Calcium participates in feedback regulation of the oscillating ROP1 Rho GTPase in pollen tubes. Proc Natl Acad Sci USA 106:22002–22007PubMedPubMedCentralCrossRefGoogle Scholar
  413. Yang Z (2002) Small GTPases: versatile signaling switches in plants. Plant Cell 14(Suppl):S375–S388PubMedPubMedCentralGoogle Scholar
  414. Yang Z (2008) Cell polarity signaling in Arabidopsis. Cell 24:551–575Google Scholar
  415. 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(10):e1074PubMedPubMedCentralCrossRefGoogle Scholar
  416. Yang X, Wang SS, Wang M, Qiao Z, Bao CC, Zhang W (2014) Arabidopsis thaliana calmodulin-like protein CML24 regulates pollen tube growth by modulating the actin cytoskeleton and controlling the cytosolic Ca2+ concentration. Plant Mol Biol 86:225–236PubMedCrossRefGoogle Scholar
  417. Ye J, Zheng Y, Yan A, Chen N, Wang Z, Huang S, Yang Z (2009) Arabidopsis formin3 directs the formation of actin cables and polarized growth in pollen tubes. Plant Cell 21:3868–3884PubMedPubMedCentralCrossRefGoogle Scholar
  418. Yi K, Guo C, Chen D, Zhao B, Yang B, Ren H (2005) Cloning and functional characterization of a formin-like protein (AtFH8) from Arabidopsis. Plant Physiol 138:1071–1082PubMedPubMedCentralCrossRefGoogle Scholar
  419. Ylstra B, Garrido D, Busscher J, van Tunen AJ (1998) Hexose transport in growing Petunia pollen tubes and characterization of a pollen-specific, putative monosaccharide transporter. Plant Physiol 118:297–304PubMedPubMedCentralCrossRefGoogle Scholar
  420. Yokota E, Muto S, Shimmen T (1999) Inhibitory regulation of higher-plant myosin by Ca2+ ions. Plant Physiol 119:231–240PubMedPubMedCentralCrossRefGoogle Scholar
  421. 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 46:1690–1703PubMedCrossRefGoogle Scholar
  422. 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 18:867–878PubMedPubMedCentralCrossRefGoogle Scholar
  423. Zabotina OA, Van De Ven WTG, Freshour G, Drakakaki G, Cavalier D, Mouille G, Hahn MG, Keegstra K, Raikhel NV (2008) Arabidopsis XXT5 gene encodes a putative alpha-1,6-xylosyltransferase that is involved in xyloglucan biosynthesis. Plant J 56:101–115PubMedCrossRefGoogle Scholar
  424. Zabotina OA, Avci U, Cavalier D, Pattathil S, Chou YH, Eberhard S, Danhof L, Keegstra K, Hahn MG (2012) Mutations in multiple XXT genes of Arabidopsis reveal the complexity of xyloglucan biosynthesis. Plant Physiol 159:1367–1384PubMedPubMedCentralCrossRefGoogle Scholar
  425. Zhang Y, McCormick S (2007) A distinct mechanism regulating a pollen-specific guanine nucleotide exchange factor for the small GTPase Rop in Arabidopsis thaliana. Proc Natl Acad Sci USA 104:18830–18835PubMedPubMedCentralCrossRefGoogle Scholar
  426. Zhang H, Qu X, Bao C, Khurana P, Wang Q, Xie Y, Zheng Y, Chen N, Blanchoin L, Staiger CJ, Huang S (2010) Arabidopsis VILLIN5, an actin filament bundling and severing protein, is necessary for normal pollen tube growth. Plant Cell 22:2749–2767PubMedPubMedCentralCrossRefGoogle Scholar
  427. Zhang Y, Xiao Y, Du F, Cao L, Dong H, Ren H (2011a) Arabidopsis VILLIN4 is involved in root hair growth through regulating actin organization in a Ca2+-dependent manner. New Phytol 190:667–682PubMedCrossRefGoogle Scholar
  428. Zhang Z, Zhang Y, Tan H, Wang Y, Li G, Liang W, Yuan Z, Hu J, Ren H, Zhang D (2011b) RICE MORPHOLOGY DETERMINANT encodes the type II formin FH5 and regulates rice morphogenesis. Plant Cell 23:681–700PubMedPubMedCentralCrossRefGoogle Scholar
  429. Zhang Y, Xie Q, Robertson JB, Johnson CH (2012) pHlash: a new genetically encoded and ratiometric luminescence sensor of intracellular pH. PLoS One 7(8):e43072PubMedPubMedCentralCrossRefGoogle Scholar
  430. Zhang X, Ma H, Qi H, Zhao J (2014) Roles of hydroxyproline-rich glycoproteins in the pollen tube and style cell growth of tobacco (Nicotiana tabacum L.). J Plant Physiol 171:1036–1045Google Scholar
  431. Zhang S, Liu C, Wang J, Ren Z, Staiger CJ, Ren H (2016) A processive Arabidopsis formin modulates actin-filament dynamics in association with profilin. Mol Plant 9:900–910PubMedCrossRefGoogle Scholar
  432. Zhao LN, Shen LK, Zhang WZ, Zhang W, Wang Y, Wu WH (2013a) Ca2+-dependent protein kinase11 and 24 modulate the activity of the inward rectifying K+ channels in Arabidopsis pollen tubes. Plant Cell 25:649–661PubMedPubMedCentralCrossRefGoogle Scholar
  433. Zhao Y, Pan Z, Zhang Y, Qu X, Zhang Y, Yang Y, Jiang X, Huang S, Yuan M, Schumaker KS, Guo Y (2013b) The actin-related Protein2 / 3 complex regulates mitochondrial-associated calcium signaling during salt stress in Arabidopsis. Plant Cell 25:4544–4559PubMedPubMedCentralCrossRefGoogle Scholar
  434. Zheng Y, Xie Y, Jiang Y, Qu X, Huang S (2013) Arabidopsis ACTIN-DEPOLYMERIZING FACTOR7 severs actin filaments and regulates actin cable turnover to promote normal pollen tube growth. Plant Cell 25:3405–3423PubMedPubMedCentralCrossRefGoogle Scholar
  435. Zhou L, Lan W, Jiang Y, Fang W, Luan S (2014) A calcium-dependent protein Kinase interacts with and activates a calcium channel to regulate pollen tube growth. Mol Plant 7:369–376PubMedCrossRefGoogle Scholar
  436. Zhou L, Lan W, Chen B, Fang W, Luan S (2015a) A calcium sensor-regulated protein kinase, CALCINEURIN B-LIKE PROTEIN-INTERACTING PROTEIN KINASE19, is required for pollen tube growth and polarity. Plant Physiol 167:1351–1360PubMedPubMedCentralCrossRefGoogle Scholar
  437. Zhou Z, Shi H, Chen B, Zhang R, Huang S, Fu Y (2015b) Arabidopsis RIC1 severs actin filaments at the apex to regulate pollen tube growth. Plant Cell 27:1140–1161PubMedPubMedCentralCrossRefGoogle Scholar
  438. Zonia L, Cordeiro S, Feijó JA (2001) Ion dynamics and hydrodynamics in the regulation of pollen tube growth. Sex Plant Reprod 14:111–116CrossRefGoogle Scholar
  439. Zorec R, Tester M (1992) Cytoplasmic calcium stimulates exocytosis in a plant secretory cell. Biophys J 63:864–867PubMedPubMedCentralCrossRefGoogle Scholar
  440. Zottini M, Zannoni D (1993) The use of Fura-2 fluorescence to monitor the movement of free calcium ions into the matrix of plant mitochondria (Pisum sativum and Helianthus tuberosus). Plant Physiol 102:573–578PubMedPubMedCentralCrossRefGoogle Scholar

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© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Biology Department, Integrated Molecular Plant Physiology ResearchUniversity of AntwerpAntwerpBelgium
  2. 2.Plant Biochemistry & Biotechnology Lab, Department of Agriculture, School of Agriculture, Food & NutritionUASC-TEICreteGreece

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