全部 标题 作者
关键词 摘要

OALib Journal期刊
ISSN: 2333-9721
费用:99美元

查看量下载量

相关文章

更多...
Plants  2013 

Calcium: The Missing Link in Auxin Action

DOI: 10.3390/plants2040650

Keywords: auxin, calcium, signal transduction, auxin transport

Full-Text   Cite this paper   Add to My Lib

Abstract:

Due to their sessile lifestyles, plants need to deal with the limitations and stresses imposed by the changing environment. Plants cope with these by a remarkable developmental flexibility, which is embedded in their strategy to survive. Plants can adjust their size, shape and number of organs, bend according to gravity and light, and regenerate tissues that were damaged, utilizing a coordinating, intercellular signal, the plant hormone, auxin. Another versatile signal is the cation, Ca 2+, which is a crucial second messenger for many rapid cellular processes during responses to a wide range of endogenous and environmental signals, such as hormones, light, drought stress and others. Auxin is a good candidate for one of these Ca 2+-activating signals. However, the role of auxin-induced Ca 2+ signaling is poorly understood. Here, we will provide an overview of possible developmental and physiological roles, as well as mechanisms underlying the interconnection of Ca 2+ and auxin signaling.

References

[1]  Vanneste, S.; Friml, J. Auxin: A trigger for change in plant development. Cell 2009, 136, 1005–1016, doi:10.1016/j.cell.2009.03.001.
[2]  Tanaka, H.; Dhonukshe, P.; Brewer, P.B.; Friml, J. Spatiotemporal asymmetric auxin distribution: A means to coordinate plant development. Cell Mol. Life Sci. 2006, 63, 2738–2754.
[3]  Napier, R.M.; Venis, M.A. Tansley review No-79-auxin action and auxin-binding proteins. New Phytol. 1995, 129, 167–201.
[4]  Bennett, T.; Scheres, B. Root development-two meristems for the price of one? Curr. Top. Dev. Biol. 2010, 91, 67–102, doi:10.1016/S0070-2153(10)91003-X.
[5]  Lavenus, J.; Goh, T.; Roberts, I.; Guyomarc’h, S.; Lucas, M.; de Smet, I.; Fukaki, H.; Beeckman, T.; Bennett, M.; Laplaze, L. Lateral root development in Arabidopsis: Fifty shades of auxin. Trends Plant Sci. 2013, 18, 450–458.
[6]  Reinhardt, D.; Pesce, E.R.; Stieger, P.; Mandel, T.; Baltensperger, K.; Bennett, M.; Traas, J.; Friml, J.; Kuhlemeier, C. Regulation of phyllotaxis by polar auxin transport. Nature 2003, 426, 255–260.
[7]  Benkova, E.; Michniewicz, M.; Sauer, M.; Teichmann, T.; Seifertova, D.; Jurgens, G.; Friml, J. Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 2003, 115, 591–602, doi:10.1016/S0092-8674(03)00924-3.
[8]  Barkoulas, M.; Hay, A.; Kougioumoutzi, E.; Tsiantis, M. A developmental framework for dissected leaf formation in the Arabidopsis relative cardamine hirsuta. Nat. Genet. 2008, 40, 1136–1141, doi:10.1038/ng.189.
[9]  Scarpella, E.; Marcos, D.; Friml, J.; Berleth, T. Control of leaf vascular patterning by polar auxin transport. Genes Dev. 2006, 20, 1015–1027, doi:10.1101/gad.1402406.
[10]  Pagnussat, G.C.; Alandete-Saez, M.; Bowman, J.L.; Sundaresan, V. Auxin-dependent patterning and gamete specification in the Arabidopsis female gametophyte. Science 2009, 324, 1684–1689.
[11]  Zadnikova, P.; Petrasek, J.; Marhavy, P.; Raz, V.; Vandenbussche, F.; Ding, Z.; Schwarzerova, K.; Morita, M.T.; Tasaka, M.; Hejatko, J.; et al. Role of pin-mediated auxin efflux in apical hook development of Arabidopsis thaliana. Development 2010, 137, 607–617.
[12]  Vandenbussche, F.; Petrasek, J.; Zadnikova, P.; Hoyerova, K.; Pesek, B.; Raz, V.; Swarup, R.; Bennett, M.; Zazimalova, E.; Benkova, E.; et al. The auxin influx carriers AUX1 and LAX3 are involved in auxin-ethylene interactions during apical hook development in Arabidopsis thaliana Seedlings. Development 2010, 137, 597–606, doi:10.1242/dev.040790.
[13]  Toyota, M.; Gilroy, S. Gravitropism and mechanical signaling in plants. Am. J. Bot. 2013, 100, 111–125, doi:10.3732/ajb.1200408.
[14]  Takahashi, H.; Miyazawa, Y.; Fujii, N. Hormonal interactions during root tropic growth: Hydrotropism versus gravitropism. Plant Mol. Biol. 2009, 69, 489–502, doi:10.1007/s11103-008-9438-x.
[15]  Friml, J.; Wisniewska, J.; Benkova, E.; Mendgen, K.; Palme, K. Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 2002, 415, 806–809.
[16]  Ding, Z.; Galvan-Ampudia, C.S.; Demarsy, E.; Langowski, L.; Kleine-Vehn, J.; Fan, Y.; Morita, M.T.; Tasaka, M.; Fankhauser, C.; Offringa, R.; et al. Light-mediated polarization of the PIN3 auxin transporter for the phototropic response in Arabidopsis. Nat. Cell Biol. 2011, 13, 447–452.
[17]  Christie, J.M.; Yang, H.; Richter, G.L.; Sullivan, S.; Thomson, C.E.; Lin, J.; Titapiwatanakun, B.; Ennis, M.; Kaiserli, E.; Lee, O.R.; et al. phot1 inhibition of ABCB19 primes lateral auxin fluxes in the shoot apex required for phototropism. PLoS Biol. 2011, 9, e1001076, doi:10.1371/journal.pbio.1001076.
[18]  Tao, Y.; Ferrer, J.L.; Ljung, K.; Pojer, F.; Hong, F.; Long, J.A.; Li, L.; Moreno, J.E.; Bowman, M.E.; Ivans, L.J.; et al. Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants. Cell 2008, 133, 164–176.
[19]  Jones, A.R.; Kramer, E.M.; Knox, K.; Swarup, R.; Bennett, M.J.; Lazarus, C.M.; Leyser, H.M.; Grierson, C.S. Auxin transport through non-hair cells sustains root-hair development. Nat. Cell Biol. 2009, 11, 78–84, doi:10.1038/ncb1815.
[20]  Ikeda, Y.; Men, S.; Fischer, U.; Stepanova, A.N.; Alonso, J.M.; Ljung, K.; Grebe, M. Local auxin biosynthesis modulates gradient-directed planar polarity in Arabidopsis. Nat. Cell Biol. 2009, 11, 731–738, doi:10.1038/ncb1879.
[21]  Irving, H.R.; Gehring, C.A.; Parish, R.W. Changes in cytosolic pH and calcium of guard cells precede stomatal movements. Proc. Natl. Acad. Sci. USA 1992, 89, 1790–1794, doi:10.1073/pnas.89.5.1790.
[22]  Ding, Z.; Wang, B.; Moreno, I.; Duplakova, N.; Simon, S.; Carraro, N.; Reemmer, J.; Pencik, A.; Chen, X.; Tejos, R.; et al. ER-localized auxin transporter PIN8 regulates auxin homeostasis and male gametophyte development in Arabidopsis. Nat. Commun. 2012, 3, doi:10.1038/ncomms1941.
[23]  Kim, J.I.; Murphy, A.S.; Baek, D.; Lee, S.W.; Yun, D.J.; Bressan, R.A.; Narasimhan, M.L. Yucca6 over-expression demonstrates auxin function in delaying leaf senescence in Arabidopsis thaliana. J. Exp. Bot. 2011, 62, 3981–3992.
[24]  Lim, P.O.; Lee, I.C.; Kim, J.; Kim, H.J.; Ryu, J.S.; Woo, H.R.; Nam, H.G. Auxin response Factor 2 (Arf2) plays a major role in regulating auxin-mediated leaf longevity. J. Exp. Bot. 2010, 61, 1419–1430.
[25]  Sorefan, K.; Girin, T.; Liljegren, S.J.; Ljung, K.; Robles, P.; Galvan-Ampudia, C.S.; Offringa, R.; Friml, J.; Yanofsky, M.F.; Ostergaard, L. A regulated auxin minimum is required for seed dispersal in Arabidopsis. Nature 2009, 459, 583–586.
[26]  Goetz, M.; Vivian-Smith, A.; Johnson, S.D.; Koltunow, A.M. Auxin response factor 8 is a negative regulator of fruit initiation in Arabidopsis. Plant Cell 2006, 18, 1873–1886, doi:10.1105/tpc.105.037192.
[27]  Ellis, C.M.; Nagpal, P.; Young, J.C.; Hagen, G.; Guilfoyle, T.J.; Reed, J.W. Auxin response factor1 and auxin response factor2 regulate senescence and floral organ abscission in Arabidopsis thaliana. Development 2005, 132, 4563–4574, doi:10.1242/dev.02012.
[28]  Grunewald, W.; Cannoot, B.; Friml, J.; Gheysen, G. parasitic nematodes modulate PIN-mediated auxin transport to facilitate infection. PLoS Pathog. 2009, 5, e1000266, doi:10.1371/journal.ppat.1000266.
[29]  Navarro, L.; Dunoyer, P.; Jay, F.; Arnold, B.; Dharmasiri, N.; Estelle, M.; Voinnet, O.; Jones, J.D. A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 2006, 312, 436–439.
[30]  Iglesias, M.J.; Terrile, M.C.; Bartoli, C.G.; D’ippolito, S.; Casalongue, C.A. Auxin signaling participates in the adaptative response against oxidative stress and salinity by interacting with redox metabolism in Arabidopsis. Plant Mol. Biol. 2010, 74, 215–222, doi:10.1007/s11103-010-9667-7.
[31]  Ding, Z.; Friml, J. Auxin regulates distal stem cell differentiation in Arabidopsis Roots. Proc. Natl. Acad. Sci. USA 2010, 107, 12046–12051, doi:10.1073/pnas.1000672107.
[32]  Himanen, K.; Boucheron, E.; Vanneste, S.; de Almeida Engler, J.; Inze, D.; Beeckman, T. Auxin-mediated cell cycle activation during early lateral root initiation. Plant Cell 2002, 14, 2339–2351, doi:10.1105/tpc.004960.
[33]  Vanneste, S.; de Rybel, B.; Beemster, G.T.; Ljung, K.; de Smet, I.; van Isterdael, G.; Naudts, M.; Iida, R.; Gruissem, W.; Tasaka, M.; et al. Cell cycle progression in the pericycle is not sufficient for solitary root/IAA14-mediated lateral root initiation in Arabidopsis thaliana. Plant Cell 2005, 17, 3035–3050.
[34]  Tromas, A.; Braun, N.; Muller, P.; Khodus, T.; Paponov, I.A.; Palme, K.; Ljung, K.; Lee, J.Y.; Benfey, P.; Murray, J.A.; et al. The auxin binding protein 1 is required for differential auxin responses mediating root growth. PLoS One 2009, 4, e6648, doi:10.1371/journal.pone.0006648.
[35]  Xu, T.; Nagawa, S.; Yang, Z. Uniform auxin triggers the rho gtpase-dependent formation of interdigitation patterns in pavement cells. Small Gtpases 2011, 2, 227–232.
[36]  Abas, L.; Benjamins, R.; Malenica, N.; Paciorek, T.; Wisniewska, J.; Moulinier-Anzola, J.C.; Sieberer, T.; Friml, J.; Luschnig, C. Intracellular Trafficking and proteolysis of the Arabidopsis auxin-efflux facilitator PIN2 are involved in root gravitropism. Nat. Cell Biol. 2006, 8, 249–256, doi:10.1038/ncb1369.
[37]  Baster, P.; Robert, S.; Kleine-Vehn, J.; Vanneste, S.; Kania, U.; Grunewald, W.; de Rybel, B.; Beeckman, T.; Friml, J. SCF(TIR1/AFB)-auxin signalling regulates PIN vacuolar trafficking and auxin fluxes during root gravitropism. EMBO J. 2013, 32, 260–274.
[38]  Paciorek, T.; Zazimalova, E.; Ruthardt, N.; Petrasek, J.; Stierhof, Y.D.; Kleine-Vehn, J.; Morris, D.A.; Emans, N.; Jurgens, G.; Geldner, N.; et al. Auxin Inhibits endocytosis and promotes its own efflux from cells. Nature 2005, 435, 1251–1256, doi:10.1038/nature03633.
[39]  Robert, S.; Kleine-Vehn, J.; Barbez, E.; Sauer, M.; Paciorek, T.; Baster, P.; Vanneste, S.; Zhang, J.; Simon, S.; Covanova, M.; Hayashi, K.; et al. ABP1 mediates auxin inhibition of clathrin-dependent endocytosis in Arabidopsis. Cell 2010, 143, 111–121, doi:10.1016/j.cell.2010.09.027.
[40]  Sauer, M.; Robert, S.; Kleine-Vehn, J. Auxin: Simply complicated. J. Exp. Bot. 2013, 64, 2565–2577, doi:10.1093/jxb/ert139.
[41]  Ljung, K. Auxin metabolism and homeostasis during plant development. Development 2013, 140, 943–950, doi:10.1242/dev.086363.
[42]  Lokerse, A.S.; Weijers, D. Auxin enters the matrix—Assembly of response machineries for specific outputs. Curr. Opin. Plant Biol. 2009, 12, 520–526, doi:10.1016/j.pbi.2009.07.007.
[43]  Chapman, E.J.; Estelle, M. Mechanism of auxin-regulated gene expression in plants. Annu. Rev. Genet. 2009, 43, 265–285, doi:10.1146/annurev-genet-102108-134148.
[44]  Vanstraelen, M.; Benkova, E. Hormonal interactions in the regulation of plant development. Annu. Rev. Cell. Dev. Biol. 2012, 28, 463–487, doi:10.1146/annurev-cellbio-101011-155741.
[45]  Bothwell, J.H.; Ng, C.K. The evolution of Ca2+ signalling in photosynthetic eukaryotes. New Phytol. 2005, 166, 21–38, doi:10.1111/j.1469-8137.2004.01312.x.
[46]  Verret, F.; Wheeler, G.; Taylor, A.R.; Farnham, G.; Brownlee, C. Calcium channels in photosynthetic eukaryotes: Implications for evolution of calcium-based signalling. New Phytol. 2010, 187, 23–43, doi:10.1111/j.1469-8137.2010.03271.x.
[47]  Hepler, P.K. Calcium: A central regulator of plant growth and development. Plant Cell 2005, 17, 2142–2155, doi:10.1105/tpc.105.032508.
[48]  Kudla, J.; Batistic, O.; Hashimoto, K. Calcium signals: The lead currency of plant information processing. Plant Cell 2010, 22, 541–563, doi:10.1105/tpc.109.072686.
[49]  Dodd, A.N.; Kudla, J.; Sanders, D. The language of calcium signaling. Annu. Rev. Plant Biol. 2010, 61, 593–620, doi:10.1146/annurev-arplant-070109-104628.
[50]  Shishova, E.; Lindberg, S. Auxin-induced cytosol acidification in wheat leaf protoplasts depends on external concentration of Ca2+. J. Plant Physiol. 1999, 155, 190–196.
[51]  Shishova, M.; Lindberg, S. Auxin induces an increase of Ca2+ concentration in the cytosol of wheat leaf protoplasts. J. Plant Physiol. 2004, 161, 937–945, doi:10.1016/j.jplph.2003.12.005.
[52]  Felle, H. Auxin causes oscillations of cytosolic free calcium and pH in Zea-Mays coleoptiles. Planta 1988, 174, 495–499, doi:10.1007/BF00634478.
[53]  Gehring, C.A.; Irving, H.R.; Parish, R.W. Effects of auxin and abscisic-acid on cytosolic calcium and ph in plant-cells. Proc. Natl. Acad. Sci. USA 1990, 87, 9645–9649.
[54]  Shishova, M.; Yemelyanov, V.; Rudashevskaya, E.; Lindberg, S. A shift in sensitivity to auxin within development of maize seedlings. J. Plant. Physiol. 2007, 164, 1323–1330, doi:10.1016/j.jplph.2006.09.005.
[55]  Monshausen, G.B.; Miller, N.D.; Murphy, A.S.; Gilroy, S. Dynamics of auxin-dependent Ca2+ and pH signaling in root growth revealed by integrating high-resolution imaging with automated computer vision-based analysis. Plant J. 2011, 65, 309–318, doi:10.1111/j.1365-313X.2010.04423.x.
[56]  Wheeler, G.L.; Brownlee, C. Ca2+ signalling in plants and green algae—Changing channels. Trends Plant Sci. 2008, 13, 506–514, doi:10.1016/j.tplants.2008.06.004.
[57]  Cousson, A.; Vavasseur, A. Putative involvement of cytosolic Ca2+ and gtp-binding proteins in cyclic-GMP-mediated induction of stomatal opening by auxin in Commelina communis L. Planta 1998, 206, 308–314, doi:10.1007/s004250050405.
[58]  Ayling, S.M.; Clarkson, D.T. The cytoplasmic streaming response of tomato root hairs to auxin; the role of calcium. Aust. J. Plant Physiol. 1996, 23, 699–708, doi:10.1071/PP9960699.
[59]  Shishova, M.F.; Lindberg, S.; Polevoi, V.V. Auxin activation of Ca2+ transport across the plasmalemma of plant cells. Russ. J. Plant Physiol. 1999, 46, 626–633.
[60]  Shishova, M.F.; Inge-Vechtomova, N.I.; Vykhvalov, K.A.; Rudashevskaya, E.L.; Polevoi, V.V. Auxin-dependent transport of K+ and Ca2+ across the membrane of plasmalemma vesicles from coleoptile cells. Russ. J. Plant. Physiol. 1998, 45, 67–73.
[61]  Thomine, S.; Zimmermann, S.; Vanduijn, B.; Barbier-Brygoo, H.; Guern, J. Calcium-channel antagonists induce direct inhibition of the outward rectifying potassium channel in tobacco protoplasts. FEBS Lett. 1994, 340, 45–50, doi:10.1016/0014-5793(94)80170-3.
[62]  Ordenes, V.R.; Moreno, I.; Maturana, D.; Norambuena, L.; Trewavas, A.J.; Orellana, A. In vivo analysis of the calcium signature in the plant Golgi apparatus reveals unique dynamics. Cell Calcium 2012, 52, 397–404, doi:10.1016/j.ceca.2012.06.008.
[63]  Krebs, M.; Held, K.; Binder, A.; Hashimoto, K.; den Herder, G.; Parniske, M.; Kudla, J.; Schumacher, K. FRET-based genetically encoded sensors allow high-resolution live cell imaging of Ca2+ Dynamics. Plant J. 2012, 69, 181–192, doi:10.1111/j.1365-313X.2011.04780.x.
[64]  Mehlmer, N.; Parvin, N.; Hurst, C.H.; Knight, M.R.; Teige, M.; Vothknecht, U.C. A toolset of aequorin expression vectors for in planta studies of subcellular calcium concentrations in Arabidopsis thaliana. J. Exp. Bot. 2012, 63, 1751–1761, doi:10.1093/jxb/err406.
[65]  Costa, A.; Drago, I.; Behera, S.; Zottini, M.; Pizzo, P.; Schroeder, J.I.; Pozzan, T.; lo Schiavo, F. H2O2 in plant peroxisomes: An in vivo analysis uncovers a Ca2+-dependent scavenging system. Plant J. 2010, 62, 760–772, doi:10.1111/j.1365-313X.2010.04190.x.
[66]  Logan, D.C.; Knight, M.R. Mitochondrial and cytosolic calcium dynamics are differentially regulated in plants. Plant Physiol. 2003, 133, 21–24, doi:10.1104/pp.103.026047.
[67]  Felle, H.; Brummer, B.; Bertl, A.; Parish, R.W. Indole-3-acetic-acid and fusicoccin cause cytosolic acidification of corn coleoptile cells. Proc. Natl. Acad. Sci. USA 1986, 83, 8992–8995, doi:10.1073/pnas.83.23.8992.
[68]  Brummer, B.; Bertl, A.; Potrykus, I.; Felle, H.; Parish, R.W. Evidence That fusicoccin and indole-3-acetic-acid induce cytosolic acidification of Zea-Mays cells. FEBS Lett. 1985, 189, 109–114, doi:10.1016/0014-5793(85)80852-8.
[69]  Jurado, S.; Abraham, Z.; Manzano, C.; Lopez-Torrejon, G.; Pacios, L.F.; Del Pozo, J.C. The Arabidopsis cell cycle f-box protein Skp2a binds to auxin. Plant Cell 2010, 22, 3891–3904, doi:10.1105/tpc.110.078972.
[70]  Sauer, M.; Kleine-Vehn, J. Auxin binding protein 1: The outsider. Plant Cell 2011, 23, 2033–2043, doi:10.1105/tpc.111.087064.
[71]  Venis, M.A.; Napier, R.M.; Oliver, S. Molecular analysis of auxin-specific signal transduction. Plant Growth Regul. 1996, 18, 1–6, doi:10.1007/BF00028481.
[72]  Barbier-Brygoo, H.; Ephritikhine, G.; Klambt, D.; Ghislain, M.; Guern, J. Functional evidence for an auxin receptor at the plasmalemma of tobacco mesophyll protoplasts. Proc. Natl. Acad. Sci. USA 1989, 86, 891–895, doi:10.1073/pnas.86.3.891.
[73]  Tian, H.; Klambt, D.; Jones, A.M. Auxin-binding protein 1 does not bind auxin within the endoplasmic reticulum despite this being the predominant subcellular location for this hormone receptor. J. Biol. Chem. 1995, 270, 26962–26969, doi:10.1074/jbc.270.45.26962.
[74]  Felle, H.; Peters, W.; Palme, K. The electrical response of maize to auxins. Biochim. Biophys. Acta 1991, 1064, 199–204.
[75]  Barbier-Brygoo, H.; Ephritikhine, G.; Klambt, D.; Maurel, C.; Palme, K.; Schell, J.; Guern, J. Perception of the auxin signal at the plasma-membrane of tobacco mesophyll protoplasts. Plant J. 1991, 1, 83–93, doi:10.1111/j.1365-313X.1991.00083.x.
[76]  Thiel, G.; Blatt, M.R.; Fricker, M.D.; White, I.R.; Millner, P. Modulation of K+ channels in vicia stomatal guard cells by peptide homologs to the auxin-binding protein C-terminus. Proc. Natl. Acad. Sci. USA 1993, 90, 11493–11497, doi:10.1073/pnas.90.24.11493.
[77]  Zimmermann, S.; Thomine, S.; Guern, J.; Barbier-Brygoo, H. An anion current at the plasma-membrane of tobacco protoplasts shows ATP-dependent voltage regulation and is modulated by auxin. Plant J. 1994, 6, 707–716.
[78]  Xu, T.; Wen, M.; Nagawa, S.; Fu, Y.; Chen, J.G.; Wu, M.J.; Perrot-Rechenmann, C.; Friml, J.; Jones, A.M.; Yang, Z. Cell surface- and rho GTPase-based auxin signaling controls cellular interdigitation in Arabidopsis. Cell 2010, 143, 99–110, doi:10.1016/j.cell.2010.09.003.
[79]  Nagawa, S.; Xu, T.; Lin, D.; Dhonukshe, P.; Zhang, X.; Friml, J.; Scheres, B.; Fu, Y.; Yang, Z. Rop GTPase-dependent actin microfilaments promote pin1 polarization by localized inhibition of clathrin-dependent endocytosis. PLoS Biol. 2012, 10, e1001299, doi:10.1371/journal.pbio.1001299.
[80]  Chen, X.; Naramoto, S.; Robert, S.; Tejos, R.; Lofke, C.; Lin, D.; Yang, Z.; Friml, J. ABP1 and ROP6 GTPase signaling regulate clathrin-mediated endocytosis in Arabidopsis roots. Curr. Biol. 2012, 22, 1326–1332, doi:10.1016/j.cub.2012.05.020.
[81]  Marten, I.; Lohse, G.; Hedrich, R. Plant-growth hormones control voltage-dependent activity of anion channels in plasma-membrane of guard-cells. Nature 1991, 353, 758–762.
[82]  Gehring, C.A.; Mcconchie, R.M.; Venis, M.A.; Parish, R.W. Auxin-binding-protein antibodies and peptides influence stomatal opening and alter cytoplasmic pH. Planta 1998, 205, 581–586, doi:10.1007/s004250050359.
[83]  Cho, D.; Villiers, F.; Kroniewicz, L.; Lee, S.; Seo, Y.J.; Hirschi, K.D.; Leonhardt, N.; Kwak, J.M. Vacuolar CAX1 and CAX3 influence auxin transport in guard cells via regulation of apoplastic pH. Plant Physiol. 2012, 160, 1293–1302, doi:10.1104/pp.112.201442.
[84]  Yamagami, M.; Haga, K.; Napier, R.M.; Iino, M. Two distinct signaling pathways participate in auxin-induced swelling of pea epidermal protoplasts. Plant Physiol. 2004, 134, 735–747, doi:10.1104/pp.103.031294.
[85]  Tromas, A.; Paque, S.; Stierle, V.; Quettier, A.L.; Muller, P.; Lechner, E.; Genschik, P.; Perrot-Rechenmann, C. Auxin-binding protein 1 is a negative regulator of the SCF(TIR1/AFB) pathway. Nat. Commun. 2013, 4, doi:10.1038/ncomms3496.
[86]  Singla, B.; Chugh, A.; Khurana, J.P.; Khurana, P. An early auxin-responsive Aux/IAA gene from wheat (Triticum aestivum) is induced by epibrassinolide and differentially regulated by light and calcium. J. Exp. Bot. 2006, 57, 4059–4070, doi:10.1093/jxb/erl182.
[87]  Thimann, K.V. Hormones and the analysis of growth. Plant Physiol. 1938, 13, 437–449, doi:10.1104/pp.13.3.437.
[88]  Takahashi, K.; Hayashi, K.; Kinoshita, T. Auxin activates the plasma membrane H+-atpase by phosphorylation during hypocotyl elongation in Arabidopsis. Plant Physiol. 2012, 159, 632–641.
[89]  Heyn, A.N.J. Molecular-Basis of auxin-regulated extension growth and role of dextranase. Proc. Natl. Acad. Sci. USA 1981, 78, 6608–6612, doi:10.1073/pnas.78.11.6608.
[90]  Heyn, A.N.J. Dextranase activity and auxin-induced cell elongation in coleoptiles of Avena. Biochem. Biophys. Res. Commun. 1970, 38, 831–837, doi:10.1016/0006-291X(70)90794-1.
[91]  Claussen, M.; Luthen, H.; Blatt, M.; Bottger, M. Auxin-induced growth and its linkage to potassium channels. Planta 1997, 201, 227–234.
[92]  Philippar, K.; Buchsenschutz, K.; Edwards, D.; Loffler, J.; Luthen, H.; Kranz, E.; Edwards, K.J.; Hedrich, R. The Auxin-induced K+ channel gene Zmk1 in maize functions in coleoptile growth and is required for embryo development. Plant Mol. Biol. 2006, 61, 757–768.
[93]  Thiel, G.; Brüdern, A.; Gradmann, D. Small inward rectifying K+ channels in coleoptiles: Inhibition by external Ca2+ and function in cell elongation. J. Membr. Biol. 1996, 149, 9–20.
[94]  Rayle, D.L.; Cleland, R.E. Evidence that auxin-induced growth of soybean hypocotyls involves proton excretion. Plant Physiol. 1980, 66, 433–437.
[95]  Hager, A. Role of the plasma membrane H+-atpase in auxin-induced elongation growth: Historical and new aspects. J. Plant Res. 2003, 116, 483–505, doi:10.1007/s10265-003-0110-x.
[96]  Luthen, H.; Bigdon, M.; Bottger, M. Reexamination of the acid growth theory of auxin action. Plant Physiol. 1990, 93, 931–939, doi:10.1104/pp.93.3.931.
[97]  Hager, A.; Menzel, H.; Krauss, A. Experiments and hypothesis concerning primary action of auxin in elongation growth. Planta 1971, 100, 47–75.
[98]  Moloney, M.M.; Elliott, M.C.; Cleland, R.E. Acid growth effects in maize roots—Evidence for a link between auxin-economy and proton extrusion in the control of root-growth. Planta 1981, 152, 285–291, doi:10.1007/BF00388251.
[99]  Tode, K.; Luthen, H. Fusicoccin- and IAA-induced elongation growth share the same pattern of K+ dependence. J. Exp. Bot. 2001, 52, 251–255, doi:10.1093/jexbot/52.355.251.
[100]  Sondergaard, T.E.; Schulz, A.; Palmgren, M.G. Energization of transport processes in plants. roles of the plasma membrane H+-atpase. Plant Physiol. 2004, 136, 2475–2482, doi:10.1104/pp.104.048231.
[101]  Duby, G.; Poreba, W.; Piotrowiak, D.; Bobik, K.; Derua, R.; Waelkens, E.; Boutry, M. Activation of plant plasma membrane H+-ATPase by 14-3-3 proteins is negatively controlled by two phosphorylation sites within the H+-ATPase C-terminal region. J. Biol. Chem. 2009, 284, 4213–4221.
[102]  Fuglsang, A.T.; Guo, Y.; Cuin, T.A.; Qiu, Q.; Song, C.; Kristiansen, K.A.; Bych, K.; Schulz, A.; Shabala, S.; Schumaker, K.S.; et al. Arabidopsis Protein Kinase PKS5 inhibits the plasma membrane H+-atpase by preventing interaction with 14-3-3 Protein. Plant Cell 2007, 19, 1617–1634.
[103]  Staal, M.; de Cnodder, T.; Simon, D.; Vandenbussche, F.; van der Straeten, D.; Verbelen, J.P.; Elzenga, T.; Vissenberg, K. Apoplastic alkalinization is instrumental for the inhibition of cell elongation in the arabidopsis root by the ethylene precursor 1-aminocyclopropane-1-carboxylic acid. Plant Physiol. 2011, 155, 2049–2055, doi:10.1104/pp.110.168476.
[104]  Hasenstein, K.H.; Evans, M.L. Calcium dependence of rapid auxin action in maize roots. Plant Physiol. 1986, 81, 439–443.
[105]  Lamport, D.T.; Varnai, P. Periplasmic arabinogalactan glycoproteins act as a calcium capacitor that regulates plant growth and development. New Phytol. 2013, 197, 58–64, doi:10.1111/nph.12005.
[106]  Schenck, D.; Christian, M.; Jones, A.; Luthen, H. Rapid auxin-induced cell expansion and gene expression: A four-decade-old question revisited. Plant Physiol. 2010, 152, 1183–1185, doi:10.1104/pp.109.149591.
[107]  Rück, A.; Palme, K.; Venis, M.A.; Napier, R.M.; Felle, R.H. Patch-clamp analysis establishes a role for an auxin-binding protein in the auxin stimulation of plasma-membrane current in Zea-mays protoplasts. Plant J. 1993, 4, 41–46.
[108]  Ivashikina, N.; Deeken, R.; Fischer, S.; Ache, P.; Hedrich, R. AKT2/3 subunits render guard cell K+ Channels Ca2+ sensitive. J. Gen. Physiol. 2005, 125, 483–492, doi:10.1085/jgp.200409211.
[109]  Cheong, Y.H.; Pandey, G.K.; Grant, J.J.; Batistic, O.; Li, L.; Kim, B.G.; Lee, S.C.; Kudla, J.; Luan, S. Two calcineurin b-like calcium sensors, interacting with protein kinase CIPK23, regulate leaf transpiration and root potassium uptake in Arabidopsis. Plant J. 2007, 52, 223–239, doi:10.1111/j.1365-313X.2007.03236.x.
[110]  Lan, W.Z.; Lee, S.C.; Che, Y.F.; Jiang, Y.Q.; Luan, S. Mechanistic analysis of AKT1 regulation by the CBL-CIPK-PP2CA interactions. Mol. Plant 2011, 4, 527–536, doi:10.1093/mp/ssr031.
[111]  Ren, X.L.; Qi, G.N.; Feng, H.Q.; Zhao, S.; Zhao, S.S.; Wang, Y.; Wu, W.H. Calcineurin B-like protein CBL10 directly interacts with AKT1 and modulates K+ homeostasis in Arabidopsis. Plant J. 2013, 74, 258–266, doi:10.1111/tpj.12123.
[112]  Li, L.; Kim, B.G.; Cheong, Y.H.; Pandey, G.K.; Luan, S. A Ca2+ signaling pathway regulates a K+ channel for low-K response in Arabidopsis. Proc. Natl. Acad. Sci. USA 2006, 103, 12625–12630.
[113]  Li, J.; Lee, Y.R.; Assmann, S.M. Guard cells possess a calcium-dependent protein kinase that phosphorylates the KAT1 potassium channel. Plant Physiol. 1998, 116, 785–795, doi:10.1104/pp.116.2.785.
[114]  Vicente-Agullo, F.; Rigas, S.; Desbrosses, G.; Dolan, L.; Hatzopoulos, P.; Grabov, A. Potassium carrier TRH1 is required for auxin transport in Arabidopsis roots. Plant J. 2004, 40, 523–535, doi:10.1111/j.1365-313X.2004.02230.x.
[115]  Rigas, S.; Ditengou, F.A.; Ljung, K.; Daras, G.; Tietz, O.; Palme, K.; Hatzopoulos, P. Root gravitropism and root hair development constitute coupled developmental responses regulated by auxin homeostasis in the arabidopsis root apex. New Phytol. 2013, 197, 1130–1141, doi:10.1111/nph.12092.
[116]  Remy, E.; Cabrito, T.R.; Baster, P.; Batista, R.A.; Teixeira, M.C.; Friml, J.; Sa-Correia, I.; Duque, P. A major facilitator superfamily transporter plays a dual role in polar auxin transport and drought stress tolerance in Arabidopsis. Plant Cell 2013, 25, 901–926, doi:10.1105/tpc.113.110353.
[117]  Tripathi, V.; Parasuraman, B.; Laxmi, A.; Chattopadhyay, D. CIPK6, A CBL-interacting protein kinase is required for development and salt tolerance in plants. Plant J. 2009, 58, 778–790, doi:10.1111/j.1365-313X.2009.03812.x.
[118]  Held, K.; Pascaud, F.; Eckert, C.; Gajdanowicz, P.; Hashimoto, K.; Corratge-Faillie, C.; Offenborn, J.N.; Lacombe, B.; Dreyer, I.; Thibaud, J.B.; et al. Calcium-dependent modulation and plasma membrane targeting of the AKT2 potassium channel by the CBL4/CIPK6 calcium sensor/protein kinase complex. Cell Res. 2011, 21, 1116–1130, doi:10.1038/cr.2011.50.
[119]  Darwin, C.; Darwin, F. The Power of Movement in Plants; Appleton and Co.: New York, NY, USA, 1881.
[120]  Marchant, A.; Bhalerao, R.; Casimiro, I.; Eklof, J.; Casero, P.J.; Bennett, M.; Sandberg, G. AUX1 promotes lateral root formation by facilitating indole-3-acetic acid distribution between sink and source tissues in the Arabidopsis Seedling. Plant Cell 2002, 14, 589–597, doi:10.1105/tpc.010354.
[121]  Tang, P.M.; Dela Fuente, R.K. The Transport of indole-3-acetic acid in boron- and calcium-deficient sunflower hypocotyl segments. Plant Physiol. 1986, 81, 646–650.
[122]  Tang, P.M.; Dela Fuente, R.K. Boron and calcium sites involved in indole-3-acetic acid transport in sunflower hypocotyl segments. Plant Physiol. 1986, 81, 651–655, doi:10.1104/pp.81.2.651.
[123]  Dela Fuente, R.K.; Leopold, A.C. Role for calcium in auxin transport. Plant Physiol. 1973, 51, 845–847, doi:10.1104/pp.51.5.845.
[124]  Evans, M.L.; Young, L.M.; Hasenstein, K.H. The role of calcium in the regulation of hormone transport in gravistimulated Roots. Adv. Space Res. 1992, 12, 211–218.
[125]  Migliaccio, F.; Galston, A.W. On the role of calcium in indole-3-acetic acid movement and graviresponse in etiolated pea epicotyls. Plant Growth Regul. 1989, 8, 335–347, doi:10.1007/BF00024664.
[126]  Raven, J.A. Transport of indole-acetic-acid in plant cells in relation to pH and electrical potential gradients, and its significance for polar IAA Transport. New Phytol. 1975, 74, 163–172, doi:10.1111/j.1469-8137.1975.tb02602.x.
[127]  Rubery, P.H.; Sheldrake, A.R. Carrier-mediated auxin transport. Planta 1974, 118, 101–121, doi:10.1007/BF00388387.
[128]  rubery, P.H.; sheldrake, A.R. Effect of pH and surface charge on cell uptake of auxin. Nature 1973, 244, 285–288, doi:10.1038/newbio244285a0.
[129]  Goldsmith, M.H.; Goldsmith, T.H.; Martin, M.H. Mathematical analysis of the chemosmotic polar diffusion of auxin through plant tissues. Proc. Natl. Acad. Sci. USA 1981, 78, 976–980, doi:10.1073/pnas.78.2.976.
[130]  Peret, B.; Swarup, K.; Ferguson, A.; Seth, M.; Yang, Y.; Dhondt, S.; James, N.; Casimiro, I.; Perry, P.; Syed, A.; et al. AUX/LAX genes encode a family of auxin influx transporters that perform distinct functions during arabidopsis development. Plant Cell 2012, 24, 2874–2885, doi:10.1105/tpc.112.097766.
[131]  Bennett, M.J.; Marchant, A.; Green, H.G.; May, S.T.; Ward, S.P.; Millner, P.A.; Walker, A.R.; Schulz, B.; Feldmann, K.A. Arabidopsis AUX1 gene: A permease-like regulator of root gravitropism. Science 1996, 273, 948–950.
[132]  Kubes, M.; Yang, H.; Richter, G.L.; Cheng, Y.; Mlodzinska, E.; Wang, X.; Blakeslee, J.J.; Carraro, N.; Petrasek, J.; Zazimalova, E.; et al. The Arabidopsis concentration-dependent influx/efflux transporter abcb4 regulates cellular auxin levels in the root epidermis. Plant J. 2012, 69, 640–654, doi:10.1111/j.1365-313X.2011.04818.x.
[133]  Krouk, G.; Lacombe, B.; Bielach, A.; Perrine-Walker, F.; Malinska, K.; Mounier, E.; Hoyerova, K.; Tillard, P.; Leon, S.; Ljung, K.; et al. Nitrate-regulated auxin transport by Nrt1.1 defines a mechanism for nutrient sensing in plants. Dev. Cell 2010, 18, 927–937, doi:10.1016/j.devcel.2010.05.008.
[134]  Yang, Y.; Hammes, U.Z.; Taylor, C.G.; Schachtman, D.P.; Nielsen, E. High-affinity auxin transport by the AUX1 influx carrier protein. Curr. Biol. 2006, 16, 1123–1127, doi:10.1016/j.cub.2006.04.029.
[135]  Swarup, R.; Kramer, E.M.; Perry, P.; Knox, K.; Leyser, H.M.; Haseloff, J.; Beemster, G.T.; Bhalerao, R.; Bennett, M.J. Root gravitropism requires lateral root cap and epidermal cells for transport and response to a mobile auxin signal. Nat. Cell Biol. 2005, 7, 1057–1065.
[136]  Swarup, K.; Benkova, E.; Swarup, R.; Casimiro, I.; Peret, B.; Yang, Y.; Parry, G.; Nielsen, E.; de Smet, I.; Vanneste, S.; et al. The auxin influx carrier Lax3 promotes lateral root emergence. Nat. Cell Biol. 2008, 10, 946–954, doi:10.1038/ncb1754.
[137]  Bainbridge, K.; Guyomarc’h, S.; Bayer, E.; Swarup, R.; Bennett, M.; Mandel, T.; Kuhlemeier, C. Auxin influx carriers stabilize phyllotactic patterning. Genes Dev. 2008, 22, 810–823, doi:10.1101/gad.462608.
[138]  Cheng, N.H.; Pittman, J.K.; Barkla, B.J.; Shigaki, T.; Hirschi, K.D. The Arabidopsis Cax1 mutant exhibits impaired ion homeostasis, development, and hormonal responses and reveals interplay among vacuolar transporters. Plant Cell 2003, 15, 347–364, doi:10.1105/tpc.007385.
[139]  Pickett, F.B.; Wilson, A.K.; Estelle, M. The Aux1 mutation of Arabidopsis confers both auxin and ethylene resistance. Plant Physiol. 1990, 94, 1462–1466, doi:10.1104/pp.94.3.1462.
[140]  Kamimoto, Y.; Terasaka, K.; Hamamoto, M.; Takanashi, K.; Fukuda, S.; Shitan, N.; Sugiyama, A.; Suzuki, H.; Shibata, D.; Wang, B.; et al. Arabidopsis ABCB21 is a facultative auxin importer/exporter regulated by cytoplasmic auxin concentration. Plant Cell Physiol. 2012, 53, 2090–2100, doi:10.1093/pcp/pcs149.
[141]  Ho, C.H.; Lin, S.H.; Hu, H.C.; Tsay, Y.F. CHL1 functions as a nitrate sensor in plants. Cell 2009, 138, 1184–1194, doi:10.1016/j.cell.2009.07.004.
[142]  Petrasek, J.; Mravec, J.; Bouchard, R.; Blakeslee, J.J.; Abas, M.; Seifertova, D.; Wisniewska, J.; Tadele, Z.; Kubes, M.; Covanova, M.; et al. PIN proteins perform a rate-limiting function in cellular auxin efflux. Science 2006, 312, 914–918, doi:10.1126/science.1123542.
[143]  Yang, H.; Murphy, A.S. Functional expression and characterization of Arabidopsis ABCB, AUX 1 and PIN auxin transporters in Schizosaccharomyces pombe. Plant J. 2009, 59, 179–191.
[144]  Blakeslee, J.J.; Bandyopadhyay, A.; Lee, O.R.; Mravec, J.; Titapiwatanakun, B.; Sauer, M.; Makam, S.N.; Cheng, Y.; Bouchard, R.; Adamec, J.; et al. Interactions among PIN-formed and P-glycoprotein auxin transporters in Arabidopsis. Plant Cell 2007, 19, 131–147, doi:10.1105/tpc.106.040782.
[145]  Mravec, J.; Kubes, M.; Bielach, A.; Gaykova, V.; Petrasek, J.; Skupa, P.; Chand, S.; Benkova, E.; Zazimalova, E.; Friml, J. Interaction of PIN and PGP transport mechanisms in auxin distribution-dependent development. Development 2008, 135, 3345–3354, doi:10.1242/dev.021071.
[146]  Henrichs, S.; Wang, B.; Fukao, Y.; Zhu, J.; Charrier, L.; Bailly, A.; Oehring, S.C.; Linnert, M.; Weiwad, M.; Endler, A.; et al. Regulation of ABCB1/PGP1-catalysed auxin transport by linker phosphorylation. EMBO J. 2012, 31, 2965–2980.
[147]  Titapiwatanakun, B.; Murphy, A.S. Post-transcriptional regulation of auxin transport proteins: Cellular trafficking, protein phosphorylation, protein maturation, ubiquitination, and membrane composition. J. Exp. Bot. 2009, 60, 1093–1107, doi:10.1093/jxb/ern240.
[148]  Cho, M.; Lee, S.H.; Cho, H.T. P-glycoprotein4 displays auxin efflux transporter-like action in Arabidopsis root hair cells and tobacco cells. Plant Cell 2007, 19, 3930–3943, doi:10.1105/tpc.107.054288.
[149]  Geisler, M.; Blakeslee, J.J.; Bouchard, R.; Lee, O.R.; Vincenzetti, V.; Bandyopadhyay, A.; Titapiwatanakun, B.; Peer, W.A.; Bailly, A.; Richards, E.L.; et al. Cellular efflux of auxin catalyzed by the arabidopsis MDR/PGP transporter AtPGP1. Plant J. 2005, 44, 179–194, doi:10.1111/j.1365-313X.2005.02519.x.
[150]  Bouchard, R.; Bailly, A.; Blakeslee, J.J.; Oehring, S.C.; Vincenzetti, V.; Lee, O.R.; Paponov, I.; Palme, K.; Mancuso, S.; Murphy, A.S.; et al. Immunophilin-like twisted DWARF1 modulates auxin efflux activities of Arabidopsis P-glycoproteins. J. Biol. Chem. 2006, 281, 30603–30612, doi:10.1074/jbc.M604604200.
[151]  Wang, B.; Bailly, A.; Zwiewka, M.; Henrichs, S.; Azzarello, E.; Mancuso, S.; Maeshima, M.; Friml, J.; Schulz, A.; Geisler, M. Arabidopsis TWISTED DWARF1 functionally interacts with auxin exporter ABCB1 on the root plasma membrane. Plant Cell 2013, 25, 202–214, doi:10.1105/tpc.112.105999.
[152]  Willige, B.C.; Ahlers, S.; Zourelidou, M.; Barbosa, I.C.; Demarsy, E.; Trevisan, M.; Davis, P.A.; Roelfsema, M.R.; Hangarter, R.; Fankhauser, C.; et al. D6PK AGCVIII kinases are required for auxin transport and phototropic hypocotyl bending in Arabidopsis. Plant Cell 2013, 25, 1674–1688, doi:10.1105/tpc.113.111484.
[153]  Benjamins, R.; Ampudia, C.S.; Hooykaas, P.J.; Offringa, R. Pinoid-mediated signaling involves calcium-binding proteins. Plant Physiol. 2003, 132, 1623–1630, doi:10.1104/pp.103.019943.
[154]  Yang, T.; Poovaiah, B.W. Molecular and biochemical evidence for the involvement of calcium/calmodulin in auxin action. J. Biol. Chem. 2000, 275, 3137–3143, doi:10.1074/jbc.275.5.3137.
[155]  Spartz, A.K.; Lee, S.H.; Wenger, J.P.; Gonzalez, N.; Itoh, H.; Inze, D.; Peer, W.A.; Murphy, A.S.; Overvoorde, P.J.; Gray, W.M. The SAUR19 subfamily of small auxin up RNA genes promote cell expansion. Plant J. 2012, 70, 978–990, doi:10.1111/j.1365-313X.2012.04946.x.
[156]  Dela Fuente, R.K. Role Of calcium in the polar secretion of indoleacetic acid. Plant Physiol. 1984, 76, 342–346, doi:10.1104/pp.76.2.342.
[157]  Grunewald, W.; Friml, J. The march of the pins: Developmental plasticity by dynamic polar targeting in plant cells. EMBO J. 2010, 29, 2700–2714, doi:10.1038/emboj.2010.181.
[158]  Cousin, M.A. Synaptic vesicle endocytosis: Calcium works overtime in the nerve terminal. Mol. Neurobiol. 2000, 22, 115–128, doi:10.1385/MN:22:1-3:115.
[159]  Dolensek, J.; Skelin, M.; Rupnik, M.S. Calcium dependencies of regulated exocytosis in different endocrine cells. Physiol. Res. 2011, 60, S29–S38.
[160]  Chrispeels, M.J.; Varner, J.E. Gibberellic acid-enhanced synthesis and release of alpha-amylase and ribonuclease by isolated barley and aleurone layers. Plant Physiol. 1967, 42, 398–406, doi:10.1104/pp.42.3.398.
[161]  Bush, D.S.; Cornejo, M.J.; Huang, C.N.; Jones, R.L. Ca-stimulated secretion of alpha-amylase during development in barley aleurone protoplasts. Plant Physiol. 1986, 82, 566–574, doi:10.1104/pp.82.2.566.
[162]  Sticher, L.; Penel, C.; Greppin, H. Calcium requirement for the secretion of peroxidases by plant cell suspensions. J. Cell Sci. 1981, 48, 345–353.
[163]  Castillo, F.J.; Penel, C.; Greppin, H. Peroxidase release induced by ozone in sedum album leaves: Involvement of Ca. Plant Physiol. 1984, 74, 846–851, doi:10.1104/pp.74.4.846.
[164]  Campanoni, P.; Blatt, M.R. Membrane trafficking and polar growth in root hairs and pollen tubes. J. Exp. Bot. 2007, 58, 65–74, doi:10.1093/jxb/erl059.
[165]  Coelho, S.M.B.; Brownlee, C.; Bothwell, J.H.F. A Tip-high, Ca2+-interdependent, reactive oxygen species gradient is associated with polarized growth in fucus serratus zygotes. Planta 2008, 227, 1037–1046, doi:10.1007/s00425-007-0678-9.
[166]  Kroeger, J.; Geitmann, A. The pollen tube paradigm revisited. Curr. Opin. Plant Biol. 2012, 15, 618–624, doi:10.1016/j.pbi.2012.09.007.
[167]  Samaj, J.; Muller, J.; Beck, M.; Bohm, N.; Menzel, D. Vesicular trafficking, cytoskeleton and signalling in root hairs and pollen tubes. Trends Plant Sci. 2006, 11, 594–600, doi:10.1016/j.tplants.2006.10.002.
[168]  Homann, U.; Tester, M. Ca2+-independent and Ca2+/GTP-binding protein-controlled exocytosis in a plant cell. Proc. Natl. Acad. Sci. USA 1997, 94, 6565–6570.
[169]  Tester, M.; Zorec, R. Cytoplasmic calcium stimulates exocytosis in a plant secretory cell. Biophys. J. 1992, 63, 864–867, doi:10.1016/S0006-3495(92)81662-4.
[170]  Sutter, J.U.; Homann, U.; Thiel, G. Ca2+-stimulated exocytosis in maize coleoptile cells. Plant Cell 2000, 12, 1127–1136.
[171]  Thiel, G.; Sutter, J.U.; Homann, U. Ca2+-sensitive and Ca2+-Insensitive exocytosis in maize coleoptile protoplasts. Pflugers Arch. 2000, 439, R152–R153, doi:10.1007/s004240000127.
[172]  Carroll, A.D.; Moyen, C.; van Kesteren, P.; Tooke, F.; Battey, N.H.; Brownlee, C. Ca2+, annexins, and gtp modulate exocytosis from maize root cap protoplast. Plant Cell 1998, 10, 1267–1276.
[173]  Sutter, J.U.; Denecke, J.; Thiel, G. Synthesis of vesicle cargo determines amplitude of Ca2+-sensitive exocytosis. Cell Calcium 2012, 52, 283–288, doi:10.1016/j.ceca.2012.05.011.
[174]  Jones, R.L.; Carbonell, J. Regulation of the synthesis of barley aleurone alpha-amylase by gibberellic acid and calcium Ions. Plant Physiol. 1984, 76, 213–218, doi:10.1104/pp.76.1.213.
[175]  Kleine-Vehn, J.; Wabnik, K.; Martiniere, A.; Langowski, L.; Willig, K.; Naramoto, S.; Leitner, J.; Tanaka, H.; Jakobs, S.; Robert, S.; et al. Recycling, clustering, and endocytosis jointly maintain PIN auxin carrier polarity at the plasma membrane. Mol. Syst. Biol. 2011, 7, doi:10.1038/msb.2011.72.
[176]  Camacho, L.; Malho, R. Endo/exocytosis in the pollen tube apex is differentially regulated by Ca2+ and GTPases. J. Exp. Bot. 2003, 54, 83–92, doi:10.1093/jxb/erg043.
[177]  Cole, R.A.; Fowler, J.E. Polarized growth: Maintaining focus on the tip. Curr. Opin. Plant Biol. 2006, 9, 579–588, doi:10.1016/j.pbi.2006.09.014.
[178]  Lee, Y.J.; Szumlanski, A.; Nielsen, E.; Yang, Z. Rho-GTPase-dependent filamentous actin dynamics coordinate vesicle targeting and exocytosis during tip growth. J. Cell Biol. 2008, 181, 1155–1168, doi:10.1083/jcb.200801086.
[179]  Xiang, Y.; Huang, X.; Wang, T.; Zhang, Y.; Liu, Q.; Hussey, P.J.; Ren, H. Actin binding protein 29 from lilium pollen plays an important role in dynamic actin remodeling. Plant Cell 2007, 19, 1930–1946, doi:10.1105/tpc.106.048413.
[180]  Ketelaar, T.; Galway, M.E.; Mulder, B.M.; Emons, A.M. Rates of exocytosis and endocytosis in arabidopsis root hairs and pollen tubes. J. Microsc. 2008, 231, 265–273, doi:10.1111/j.1365-2818.2008.02031.x.
[181]  Derksen, J.; Rutten, T.; Lichtscheidl, I.K.; Dewin, A.H.N.; Pierson, E.S.; Rongen, G. Quantitative-analysis of the distribution of organelles in tobacco pollen tubes—Implications for exocytosis and endocytosis. Protoplasma 1995, 188, 267–276, doi:10.1007/BF01280379.
[182]  Lisboa, S.; Scherer, G.E.; Quader, H. Localized endocytosis in tobacco pollen tubes: Visualisation and dynamics of membrane retrieval by a fluorescent phospholipid. Plant Cell Rep. 2008, 27, 21–28, doi:10.1007/s00299-007-0437-1.
[183]  Moscatelli, A.; Ciampolini, F.; Rodighiero, S.; Onelli, E.; Cresti, M.; Santo, N.; Idilli, A. Distinct endocytic pathways identified in tobacco pollen tubes using charged nanogold. J. Cell Sci. 2007, 120, 3804–3819, doi:10.1242/jcs.012138.
[184]  Moscatelli, A.; Idilli, A.I.; Rodighiero, S.; Caccianiga, M. Inhibition of actin polymerisation by low concentration latrunculin B affects endocytosis and alters exocytosis in shank and tip of tobacco pollen tubes. Plant Biol. 2012, 14, 770–782, doi:10.1111/j.1438-8677.2011.00547.x.
[185]  Zonia, L.; Munnik, T. Vesicle trafficking dynamics and visualization of zones of exocytosis and endocytosis in tobacco pollen tubes. J. Exp. Bot. 2008, 59, 861–873, doi:10.1093/jxb/ern007.
[186]  Wabnik, K.; Govaerts, W.; Friml, J.; Kleine-Vehn, J. Feedback models for polarized auxin transport: An emerging trend. Mol. Biosyst. 2011, 7, 2352–2359, doi:10.1039/c1mb05109a.
[187]  Wu, Y.; Zhao, S.; Tian, H.; He, Y.; Xiong, W.; Guo, L. CPK3-phosphorylated RhoGDI1 is essential in the development of Arabidopsis seedlings and leaf epidermal cells. J. Exp. Bot. 2013, 64, 3327–3338, doi:10.1093/jxb/ert171.
[188]  Lee, Y.J.; Yang, Z. Tip growth: Signaling in the apical dome. Curr. Opin. Plant Biol. 2008, 11, 662–671, doi:10.1016/j.pbi.2008.10.002.
[189]  Marhavy, P.; Bielach, A.; Abas, L.; Abuzeineh, A.; Duclercq, J.; Tanaka, H.; Parezova, M.; Petrasek, J.; Friml, J.; Kleine-Vehn, J.; et al. Cytokinin modulates endocytic trafficking of PIN1 auxin efflux carrier to control plant organogenesis. Dev. Cell 2011, 21, 796–804, doi:10.1016/j.devcel.2011.08.014.
[190]  Shinohara, N.; Taylor, C.; Leyser, O. Strigolactone can promote or inhibit shoot branching by triggering rapid depletion of the auxin efflux protein PIN1 from the plasma membrane. PLoS Biol. 2013, 11, e1001474, doi:10.1371/journal.pbio.1001474.
[191]  L?fke, C.; Zwiewka, M.; Heilmann, I.; van Montagu, M.C.; Teichmann, T.; Friml, J. Asymmetric gibberellin signaling regulates vacuolar trafficking of PIN auxin transporters during root gravitropism. Proc. Natl. Acad. Sci. USA 2013, 110, 3627–3632.
[192]  Willige, B.C.; Isono, E.; Richter, R.; Zourelidou, M.; Schwechheimer, C. Gibberellin regulates PIN-formed abundance and is required for auxin transport-dependent growth and development in Arabidopsis thaliana. Plant Cell 2011, 23, 2184–2195, doi:10.1105/tpc.111.086355.
[193]  Du, Y.; Tejos, R.; Beck, M.; Himschoot, E.; Li, H.; Robatzek, S.; Vanneste, S.; Friml, J. Salicylic acid interferes with clathrin-mediated endocytic protein trafficking. Proc. Natl. Acad. Sci. USA 2013, 110, 7946–7951, doi:10.1073/pnas.1220205110.
[194]  Feraru, E.; Friml, J. PIN polar targeting. Plant Physiol. 2008, 147, 1553–1559, doi:10.1104/pp.108.121756.
[195]  Wisniewska, J.; Xu, J.; Seifertova, D.; Brewer, P.B.; Ruzicka, K.; Blilou, I.; Rouquie, D.; Benkova, E.; Scheres, B.; Friml, J. Polar PIN localization directs auxin flow in plants. Science 2006, 312, doi:10.1126/science.1121356.
[196]  Friml, J.; Vieten, A.; Sauer, M.; Weijers, D.; Schwarz, H.; Hamann, T.; Offringa, R.; Jurgens, G. Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 2003, 426, 147–153, doi:10.1038/nature02085.
[197]  Rakusova, H.; Gallego-Bartolome, J.; Vanstraelen, M.; Robert, H.S.; Alabadi, D.; Blazquez, M.A.; Benkova, E.; Friml, J. Polarization of PIN3-dependent auxin transport for hypocotyl gravitropic response in Arabidopsis thaliana. Plant J. 2011, 67, 817–826, doi:10.1111/j.1365-313X.2011.04636.x.
[198]  Sauer, M.; Balla, J.; Luschnig, C.; Wisniewska, J.; Reinohl, V.; Friml, J.; Benkova, E. Canalization of auxin flow by AUX/IAA-ARF-dependent feedback regulation of PIN polarity. Genes Dev. 2006, 20, 2902–2911, doi:10.1101/gad.390806.
[199]  Huang, F.; Zago, M.K.; Abas, L.; van Marion, A.; Galvan-Ampudia, C.S.; Offringa, R. Phosphorylation of conserved PIN motifs directs arabidopsis pin1 polarity and auxin transport. Plant Cell 2010, 22, 1129–1142, doi:10.1105/tpc.109.072678.
[200]  Zhang, J.; Nodzynski, T.; Pencik, A.; Rolcik, J.; Friml, J. PIN Phosphorylation is sufficient to mediate pin polarity and direct auxin transport. Proc. Natl. Acad. Sci. USA 2010, 107, 918–922, doi:10.1073/pnas.0909460107.
[201]  Friml, J.; Yang, X.; Michniewicz, M.; Weijers, D.; Quint, A.; Tietz, O.; Benjamins, R.; Ouwerkerk, P.B.; Ljung, K.; Sandberg, G.; et al. A pinoid-dependent binary switch in apical-basal PIN polar targeting directs auxin efflux. Science 2004, 306, 862–865, doi:10.1126/science.1100618.
[202]  Michniewicz, M.; Zago, M.K.; Abas, L.; Weijers, D.; Schweighofer, A.; Meskiene, I.; Heisler, M.G.; Ohno, C.; Zhang, J.; Huang, F.; et al. Antagonistic regulation of pin phosphorylation by PP2A and PINOID directs auxin flux. Cell 2007, 130, 1044–1056, doi:10.1016/j.cell.2007.07.033.
[203]  Kleine-Vehn, J.; Huang, F.; Naramoto, S.; Zhang, J.; Michniewicz, M.; Offringa, R.; Friml, J. PIN auxin efflux carrier polarity is regulated by pinoid kinase-mediated recruitment into GNOM-independent trafficking in Arabidopsis. Plant Cell 2009, 21, 3839–3849, doi:10.1105/tpc.109.071639.
[204]  Babourina, O.; Newman, I.; Shabala, S. Blue light-induced kinetics of H+ and Ca2+ fluxes in etiolated wild-type and phototropin-mutant arabidopsis seedlings. Proc. Natl. Acad. Sci. USA 2002, 99, 2433–2438, doi:10.1073/pnas.042294599.
[205]  Chen, X.; Lin, W.H.; Wang, Y.; Luan, S.; Xue, H.W. An inositol polyphosphate 5-phosphatase functions in phototropin1 signaling in Arabidopis by altering cytosolic Ca2+. Plant Cell 2008, 20, 353–366, doi:10.1105/tpc.107.052670.
[206]  Perera, I.Y.; Hung, C.Y.; Brady, S.; Muday, G.K.; Boss, W.F. A universal role for inositol 1,4,5-trisphosphate-mediated signaling in plant gravitropism. Plant Physiol. 2006, 140, 746–760, doi:10.1104/pp.105.075119.
[207]  Zhang, J.; Vanneste, S.; Brewer, P.B.; Michniewicz, M.; Grones, P.; Kleine-Vehn, J.; Lofke, C.; Teichmann, T.; Bielach, A.; Cannoot, B.; et al. Inositol trisphosphate-induced Ca2+ signaling modulates auxin transport and PIN polarity. Dev. Cell 2011, 20, 855–866, doi:10.1016/j.devcel.2011.05.013.
[208]  Gehring, C.A.; Williams, D.A.; Cody, S.H.; Parish, R.W. Phototropism and geotropism in maize coleoptiles are spatially correlated with increases in cytosolic free calcium. Nature 1990, 345, 528–530, doi:10.1038/345528a0.
[209]  Plieth, C.; Trewavas, A.J. Reorientation of seedlings in the earth’s gravitational field induces cytosolic calcium transients. Plant Physiol. 2002, 129, 786–796, doi:10.1104/pp.011007.
[210]  Toyota, M.; Furuichi, T.; Tatsumi, H.; Sokabe, M. Cytoplasmic calcium increases in response to changes in the gravity vector in hypocotyls and petioles of Arabidopsis seedlings. Plant Physiol. 2008, 146, 505–514.
[211]  Band, L.R.; Wells, D.M.; Larrieu, A.; Sun, J.; Middleton, A.M.; French, A.P.; Brunoud, G.; Sato, E.M.; Wilson, M.H.; Peret, B.; et al. Root gravitropism is regulated by a transient lateral auxin gradient controlled by a tipping-point mechanism. Proc. Natl. Acad. Sci. USA 2012, 109, 4668–4673.
[212]  Lee, J.S.; Mulkey, T.J.; Evans, M.L. Inhibition of polar calcium movement and gravitropism in roots treated with auxin-transport inhibitors. Planta 1984, 160, 536–543, doi:10.1007/BF00411142.
[213]  Lee, J.S.; Mulkey, T.J.; Evans, M.L. Gravity-induced polar transport of calcium across root tips of maize. Plant Physiol. 1983, 73, 874–876, doi:10.1104/pp.73.4.874.
[214]  Bjorkman, T.; Leopold, A.C. Effect of inhibitors of auxin transport and of calmodulin on a gravisensing-dependent current in maize roots. Plant Physiol. 1987, 84, 847–850, doi:10.1104/pp.84.3.847.
[215]  Lee, J.S.; Mulkey, T.J.; Evans, M.L. Reversible loss of gravitropic sensitivity in maize roots after tip application of calcium chelators. Science 1983, 220, 1375–1376.
[216]  Friedman, H.; Meir, S.; Rosenberger, I.; Halevy, A.H.; Kaufman, P.B.; Philosoph-Hadas, S. Inhibition of the gravitropic response of snapdragon spikes by the calcium-channel blocker lanthanum chloride. Plant Physiol. 1998, 118, 483–492, doi:10.1104/pp.118.2.483.
[217]  Daye, S.; Biro, R.L.; Roux, S.J. Inhibition of gravitropism in oat coleoptiles by the calcium chelator, ethyleneglycol-bis-(beta-aminoethyl ether)-N,N'-tetraacetic acid. Plant Physiol. 1984, 61, 449–454, doi:10.1111/j.1399-3054.1984.tb06354.x.
[218]  Biro, R.L.; Hale, C.C.; Wiegand, O.F.; Roux, S.J. Effects of chlorpromazine on gravitropism in avena coleoptiles. Ann. Bot. 1982, 50, 737–745.
[219]  Stinemetz, C.L.; Kuzmanoff, K.M.; Evans, M.L.; Jarrett, H.W. Correlation between calmodulin activity and gravitropic sensitivity in primary roots of maize. Plant Physiol. 1987, 84, 1337–1342, doi:10.1104/pp.84.4.1337.
[220]  Baldwin, K.L.; Strohm, A.K.; Masson, P.H. Gravity Sensing and signal transduction in vascular plant primary roots. Am. J. Bot. 2013, 100, 126–142, doi:10.3732/ajb.1200318.
[221]  Kleine-Vehn, J.; Ding, Z.; Jones, A.R.; Tasaka, M.; Morita, M.T.; Friml, J. Gravity-induced PIN transcytosis for polarization of auxin fluxes in gravity-sensing root cells. Proc. Natl. Acad. Sci. USA 2010, 107, 22344–22349.
[222]  Ottenschlager, I.; Wolff, P.; Wolverton, C.; Bhalerao, R.P.; Sandberg, G.; Ishikawa, H.; Evans, M.; Palme, K. Gravity-regulated differential auxin transport from columella to lateral root cap cells. Proc. Natl. Acad. Sci. USA 2003, 100, 2987–2991.
[223]  Luschnig, C.; Gaxiola, R.A.; Grisafi, P.; Fink, G.R. Eir1, a root-specific protein involved in auxin transport, is required for gravitropism in Arabidopsis thaliana. Genes Dev. 1998, 12, 2175–2187, doi:10.1101/gad.12.14.2175.

Full-Text

comments powered by Disqus

Contact Us

service@oalib.com

QQ:3279437679

WhatsApp +8615387084133