Proton pump and plant cell elongation

  • Anastasia Kirpichnikova Department of Plant Physiology and Biochemistry, Faculty of Biology, Saint Petersburg State University, Universitetskaya nab., 7–9, Saint Petersburg, 199034, Russian Federation https://orcid.org/0000-0001-5133-5175
  • Tingzhuo Chen Department of Plant Physiology and Biochemistry, Faculty of Biology, Saint Petersburg State University, Universitetskaya nab., 7–9, Saint Petersburg, 199034, Russian Federation https://orcid.org/0000-0001-5143-6128
  • Serafima Teplyakova Department of Plant Physiology and Biochemistry, Faculty of Biology, Saint Petersburg State University, Universitetskaya nab., 7–9, Saint Petersburg, 199034, Russian Federation
  • Maria Shishova Department of Plant Physiology and Biochemistry, Faculty of Biology, Saint Petersburg State University, Universitetskaya nab., 7–9, Saint Petersburg, 199034, Russian Federation https://orcid.org/0000-0003-3657-2986

Abstract

Plant cell elongation growth is an integral process involved in different plant movements (tropisms); it provides the possibility to reach different resources of energy, water and nutrition and is therefore important for metabolism and development. Cell multiple enlargement along the longitudinal axis is commonly accepted to be under the control of the phytohormone auxin. One of the key enzymes involved in elongation is the plasma membrane H+-ATPase, which is known to acidify the cell wall. Investigation of the role of the proton pump at the plasma membrane was initiated by Prof. Vsevolod V. Polevoi and still is in progress in the group of Prof. Maria F. Shishova at the Department of Plant Physiology and Biochemistry, St. Petersburg State University. Different mechanisms of post-translation regulation of H+-pump activity are discussed in this review. We also suggest a possible scheme of elongation growth based on the shift in plant cell sensitivity to auxin and on its facility to elongate.

Keywords:

H -pump, plasma membrane, elongation growth, auxin, phosphorylation, exocytosis

Downloads

Download data is not yet available.
 

References

Abel, S., Oeller, P. W., and Theologis, A. 1994. Early auxin-induced genes encode short-lived nuclear proteins. Proceedings of the National Academy of Sciences of the USA 91(1):326–330. https://doi.org/10.1073/pnas.91.1.326

Anzi, C., Pelucchi, P., Vazzola, V., Murgia, I., Gomarasca, S., Beretta Piccoli, M., and Morandini, P. 2008. The proton pump interactor (Ppi) gene family of Arabidopsis thaliana: expression pattern of Ppi1 and characterization of knockout mutants for Ppi1 and 2. Plant Biology 10(2):237–249. https://doi.org/10.1111/j.1438-8677.2007.00022.x

Ayling, S. M. and Clarkson, D. T. 1996. The cytoplasmic streaming response of tomato root hairs to auxin: The role of calcium. Australian Journal of Plant Physiology 23(6):699–708. https://doi.org/10.1071/PP9960699

Babakov, A. V., Chelysheva, V. V., Klychnikov, O. I., Zorinyanz, S. E., Trofimova, M. S., and De Boer, A. H. 2000. Involvement of 14–3–3 proteins in the osmotic regulation of H+-ATPase in plant plasma membranes. Planta 211(3):446–448. https://doi.org/10.1007/s004250000347

Barbier-Brygoo, H. 1995. Tracking auxin receptors using functional approaches. Critical Reviews in Plant Sciences 14(1):1–25. https://doi.org/10.1080/07352689509701920

Barbier-Brygoo, H., Ephritikhine, G., Klämbt, D., Ghislain, M., and Guern, J. 1989. Functional evidence for an auxin receptor at the plasmalemma of tobacco mesophyll protoplasts. Proceedings of the National Academy of Sciences of the USA 86(3):891–895. https://doi.org/10.1073/pnas.86.3.891

Barbier-Brygoo, H., Ephritikhine, G., Klämbt, D., Maurel, C., Palme, K., Schell, J., and Guern, J. 1991. Perception of the auxin signal at the plasma membrane of tobacco mesophyll protoplasts. Plant Journal 1(1):83–93. https://doi.org/10.1111/j.1365-313X.1991.00083.x

Battey, N. H., James, N. C., Greenland, A. J., and Brownlee C. 1999. Exocytosis and endocytosis. Plant Cell 11(4):643–659. https://doi.org/10.1105/tpc.11.4.643

Baxter, I., Tchieu, J., Sussman, M. R., Boutry, M., Palmgren, M. G., Gribskov, M., Harper, J. F., and Axelsen, K. B. 2003. Genomic comparison of P-type ATPase ion pumps in Arabidopsis and rice. Plant Physiology 132(2):618–628. https://doi.org/10.1104/pp.103.021923

Bonza, M. C., Fusca, T., Homann, U., Thiel, G., and De Michelis, M. I. 2009. Intracellular localisation of PPI1 (proton pump interactor, isoform 1), a regulatory protein of the plasma membrane H+-ATPase of Arabidopsis thaliana. Plant Biology 11(6):869-877. https://doi.org/10.1111/j.1438-8677.2008.00181.x

Brault, M., Amiar, Z., Pennarun, A. M., Monestiez, M., Zhang, Z., Cornel, D., and Rona, J. P. 2004. Plasma membrane depolarization induced by abscisic acid in Arabidopsis suspension cells involves reduction of proton pumping in addition to anion channel activation, which are both Ca2+ dependent. Plant Physiology 135(1):231–243. https://doi.org/10.1104/pp.104.039255

Caesar, K., Elgass, K., Chen, Z., Huppenberger, P., Witthöft, J., Schleifenbaum, F., and Harter, K. 2011. A fast brassinolide-regulated response pathway in the plasma membrane of Arabidopsis thaliana. Plant Journal 66(3):528–540. https://doi.org/10.1111/j.1365-313X.2011.04510.x

Chae, K., Isaacs, C. G., Reeves, P. H., Maloney, G. S., Muday, G. K., Nagpal, P., and Reed, J. W. 2012. Arabidopsis SMALL AUXIN UP RNA63 promotes hypocotyl and stamen filament elongation. Plant Journal 71(4):684–697. https://doi.org/10.1111/j.1365-313X.2012.05024.x

Chelysheva, V. V., Smolenskaya, I. N., Trofimova, M. C., Babakov, A. V., and Muromtsev, G. S. 1999. Role of the 14-3-3 proteins in the regulation of H+-ATPase activity in the plasma membrane of suspension-cultured sugar beet cells under cold stress. FEBS Letters 456(1):22–26. https://doi.org/10.1016/S0014-5793(99)00923-0

Chen, J.-G., Shimomura S., Sitbon, F., Sandberg, G., and Jones, A. M. 2001. The role of auxin-binding protein 1 in the expansion of tobacco leaf cells. Plant Journal 28(6):607–617. https://doi.org/10.1046/j.1365-313x.2001.01152.x

Chen, Y., Hao, X., and Cao, J. 2014. Small auxin upregulated RNA (SAUR) gene family in maize: identification, evolution, and its phylogenetic comparison with Arabidopsis, rice, and sorghum. Journal of Integrative Plant Biology 56(2):133–150. https://doi.org/10.1111/jipb.12127

Christian, M., Steffens, B., Schenck, D., Burmester, S., Böttger, M., and Lüthen. H. 2006. How does auxin enhance cell elongation? Role of auxin-binding proteins and potassium channels in growth control. Plant Biology 8(3):346–352. https://doi.org/10.1055/s-2006-923965

Cleland, R. 1971. Cell wall extension. Annual Review of Plant Physiology 22:197–222. https://doi.org/10.1146/annurev.pp.22.060171.001213

Duby, G. and Boutry, M. 2009. The plant plasma membrane proton pump ATPase: a highly regulated P-type ATPase with multiple physiological roles. Pflügers Archiv-European Journal of Physiology 457(3):645–655. https://doi.org/10.1007/s00424-008-0457-x

Falhof, J., Pedersen, J. T., Fuglsang, A. T., and Palmgren, M. 2016. Plasma membrane H+-ATPase regulation in the center of plant physiology. Molecular Plant 9(3):323–337. https://doi.org/10.1016/j.molp.2015.11.002

Felle, H. 1988. Auxin causes oscillations of cytosolic free calcium and pH in Zea mays coleoptiles. Planta 174(4):495–499. https://doi.org/10.1007/BF00634478

Felle, H. H. 2001. pH: Signal and messenger in plant cells. Plant Biology 3(6):577–591. https://doi.org/10.1055/s-2001-19372

Felle, H., Brummer, B., Bertl, A., and Parish, R. W. 1986. Indole-3-acetic acid and fusicoccin cause cytosolic acidification of corn coleoptile cells. Proceedings of the National Academy of Sciences of the USA 83(23):8992–8995. https://doi.org/10.1073/pnas.83.23.8992

Felle, H., Peters, W., and Palme, K. 1991. The electrical response of maize to auxins. Biochimica et Biophysica Acta 1064(2):199–204. https://doi.org/10.1016/0005-2736(91)90302-O

Fendrych, M., Leung, J., and Friml, J. 2016. TIR1/AFB-Aux/IAA auxin perception mediates rapid cell wall acidification and growth of Arabidopsis hypocotyls. eLife 5:e19048. https://doi.org/10.7554/eLife.19048

Ferl, R. J. 2004. 14-3-3 proteins: regulation of signal-induced events. Physiologia Plantarum 120(2):173–178. https://doi.org/10.1111/j.0031-9317.2004.0239.x

Fuglsang, A. T., Guo, Y., Cuin, T. A., Qiu, Q., Song, C., Kristiansen, K. A., Bych, K., Schulz, A., Shabala, S., Schumaker, K. S., Palmgren, M. G., and Zhu, J.-K. 2007. Arabidopsis protein kinase PKS5 inhibits the plasma membrane H+-ATPase by preventing interaction with 14-3-3 protein. Plant Cell 19(5):1617–1634. https://doi.org/10.1105/tpc.105.035626

Fuglsang, A. T., Tulinius, G., Cui, N., and Palmgren, M. G. 2006. Protein phosphatase 2A scaffolding subunit A interacts with plasma membrane H+-ATPase C-terminus in the same region as 14-3-3 protein. Physiologia Plantarum 128(2):334–340. https://doi.org/10.1111/j.1399-3054.2006.00757.x

Gao, Y., Zhang, Y., Zhang, D., Dai, X., Estelle, M. and Zhao, Y. 2015. Auxin binding protein 1 (ABP1) is not required for either auxin signaling or Arabidopsis development. Proceedings of the National Academy of Sciences of the USA 112(7):2275–2280. https://doi.org/10.1073/pnas.1500365112

Gaxiola, R. A., Palmgren, M. G., and Schumacher, K. 2007. Plant proton pumps. FEBS Letters 581(12):2204–2214. https://doi.org/10.1016/j.febslet.2007.03.050

Gehring, C. A., Irving, H., and Parish, R. W. 1990. Effects of auxin and abscisic acid on cytosolic calcium and pH in plant cells. Proceedings of the National Academy of Sciences of the USA 87(24):9645–9649. https://doi.org/10.1073/pnas.87.24.9645

Grones, P. and Friml, J. 2015. ABP1: finally docking. Molecular Plant 8(3):356–358. https://doi.org/10.1016/j.molp.2014.12.013

Hagen, G. and Guilfoyle, T. 2002. Auxin-responsive gene expression: genes, promoters and regulatory factors. Plant Molecular Biology 49(3–4):373–385. https://doi.org/10.1023/A:1015207114117

Hager, A., Debus, G., Edel, H. G., Stransky, H., and Serrano, R. 1991. Auxin induces exocytosis and the rapid synthesis of a high-turnover pool of plasma-membrane H+-ATPase. Planta 185(4):527–537. https://doi.org/10.1007/BF00202963

Hager, A., Menzel, H., and Krauss, A. 1971. Experiments and hypothesis concerning the primary action of auxin in elongation growth. Planta 100(1):47–75. https://doi.org/10.1007/BF00386886

Hager, A. and Moser, I. 1985. Acetic acid esters and permeable weak acids induce active proton extrusion and extension growth of coleoptile segments by lowering the cytoplasmic pH. Planta 163(3):391–400. https://doi.org/10.1007/BF00395148

Haruta, M., Burch, H. L., Nelson, R. B., Barrett-Wilt, G., Kline, K. G., Mohsin, S. B., and Sussman, M. R. 2010. Molecular characterization of mutant Arabidopsis plants with reduced plasma membrane proton pump activity. Journal of Biological Chemistry 285(23):17918–17929. https://doi.org/10.1074/jbc.M110.101733

Haruta, M., Gray, W. M., and Sussman, M. R. 2015. Regulation of the plasma membrane proton pump (H+-ATPase) by phosphorylation. Current Opinion in Plant Biology 28:68–75. https://doi.org/10.1016/j.pbi.2015.09.005

Hayashi, M., Inoue, S. I., Takahashi, K., and Kinoshita, T. 2011. Immunohistochemical detection of blue light-induced phosphorylation of the plasma membrane H+-ATPase in stomatal guard cells. Plant and Cell Physiology 52(7):1238–1248. https://doi.org/10.1093/pcp/pcr072

Hayashi, Y., Takahashi, K., Inoue, S. I., and Kinoshita, T. 2014. Abscisic acid suppresses hypocotyl elongation by dephosphorylating plasma membrane H+-ATPase in Arabidopsis thaliana. Plant and Cell Physiology 55(4):845–853. https://doi.org/10.1093/pcp/pcu028

Hwang, J. U., Gu, Y., Lee, Y. J., and Yang, Z. 2005. Oscillatory ROP GTPase activation leads the oscillatory polarized growth of pollen tubes. Molecular Biology of the Cell 16(11):5385–5399. https://doi.org/10.1091/mbc.E05-05-0409

Irving, H., Gehring, C. A., and Parish, R. W. 1992. Changes in cytosolic pH and calcium of guard cells precede stomatal movements. Proceedings of the National Academy of Sciences of the USA 89(5):1790–1794. https://doi.org/10.1073/pnas.89.5.1790

Jones, A. M. and Herman, E. 1993. KDEL-containing auxinbinding protein is secreted to the plasma membrane and cell wall. Plant Physiology 101(2):595–606. https://doi.org/10.1104/pp.101.2.595

Kasamo, K. 2003. Regulation of plasma membrane H+-ATPase activity by the membrane environment. Journal of Plant Research 116(6):517–523. https://doi.org/10.1007/s10265-003-0112-8

Kim, Y.-S., Kim, D., and Jung, J. 2000. Two isoforms of soluble auxin receptor in rice (Oryza sativa L.) plants: binding property for auxin and interaction with plasma membrane H+-ATPase. Plant Growth Regulation 32(2-3):143–150. https://doi.org/10.1023/A:1010745310101

Kim, Y.-S., Min, J. K., Kim, D., and Jung, J. 2001. A soluble auxinbinding protein, ABP57 purification with anti-bovine serum albumin antibody and characterization of its mechanistic role in the auxin effect on plant plasma membrane H+-ATPase. Journal of Biological Chemistry 276(14):10730–10736. https://doi.org/10.1074/jbc.M009416200

Kinoshita, T., and Shimazaki, K.-I. 2001. Analysis of the phosphorylation level in guard-cell plasma membrane H+-ATPase in response to fusicoccin. Plant and Cell Physiology 42(4):424–432. https://doi.org/10.1093/pcp/pce055

Kirpichnikova, A. A., Rudashevskaya, E. L., Yemelyanov, V. V., and Shishova, M. F. 2014. Ca2+-transport through plasma membrane as a test of auxin sensitivity. Plants 3(2):209–222. https://doi.org/10.3390/plants3020209

Klambt D. 1990. A view about the function of auxin-binding proteins at plasma membranes. Plant Molecular Biology 14(6):1045–1050. https://doi.org/10.1007/BF00019401

Knauss, S., Rohrmeier, T., and Lehle, L. 2003. The auxin-induced maize gene ZmSAUR2 encodes a short-lived nuclear protein expressed in elongating tissues. Journal of Biological Chemistry 278(26):23936–23943. https://doi.org/10.1074/jbc.M212585200

Li, X., Liu, G., Geng, Y., Wu, M., Pei, W., Zhai, H., Zang, X., Li, X., Zhang, J., Yu, Sh., Yu, J. 2017. A genome-wide analysis of the small auxin up RNA (SAUR) gene family in cotton. BMC Genomics 18:815–837. https://doi.org/10.1186/s12864-017-4224-2

MacDonald, H. 1997. Auxin perception and signal transduction. Physiologia Plantarum 100(3):423–430. https://doi.org/10.1111/j.1399-3054.1997.tb03046.x

Michalko, J., Dravecka, M., Bollenbach, T., and Friml, J. 2015. Embryo-lethal phenotypes in early abp1 mutants are due to disruption of the neighboring BSM gene. F1000Research 4:1104. https://doi.org/10.12688/f1000research.7143.1

Michalko, J., Glanc, M., Perrot-Rechenmann, C., and Friml, J. 2016. Strong morphological defects in conditional Arabidopsis abp1 knock-down mutants generated in absence of functional ABP1 protein. F1000Research 5:86. https://doi.org/10.12688/f1000research.7654.1

Monshausen, G. B., Miller, N. D., Murphy, A. S., and Gilroy, S. 2011. Dynamics of auxin-dependent Ca2+ and pH signaling in root growth revealed by integrating highresolution imaging with automated computer visionbased analysis. Plant Journal 65(2):309–318. https://doi.org/10.1111/j.1365-313X.2010.04423.x

Morales-Cedillo, F., González-Solís, A., Gutiérrez-Angoa, L., Cano-Ramírez, D. L., and Gavilanes-Ruiz, M. 2015. Plant lipid environment and membrane enzymes: the case of the plasma membrane H+-ATPase. Plant Cell Reports 34(4):617–629. https://doi.org/10.1007/s00299-014-1735-z

Morandini, P., Valera, M., Albumi, C., Bonza, M. C., Giacometti, S., Ravera, G., and De Michelis, M. I. 2002. A novel interaction partner for the C-terminus of Arabidopsis thaliana plasma membrane H+-ATPase (AHA1 isoform): site and mechanism of action on H+-ATPase activity differ from those of 14-3-3 proteins. Plant Journal 31(4):487–497. https://doi.org/10.1046/j.1365-313X.2002.01373.x

Morth, J. P., Pedersen, B. P., Buch-Pedersen, M. J., Andersen, J. P., Vilsen, B., Palmgren, M. G., and Nissen, P. 2011. A structural overview of the plasma membrane Na+, K+-ATPase and H+-ATPase ion pumps. Nature Reviews Molecular Cell Biology 12:60–70. https://doi.org/10.1038/nrm3031

Murphy, A. S., and Peer, W. A. 2012. Vesicle trafficking: ROPRIC round about. Current Biology 22(14):R576–R578. https://doi.org/10.1016/j.cub.2012.06.008

Nühse, T. S., Bottrill, A. R., Jones, A. M., and Peck, S. C. 2007. Quantitative phosphoproteomic analysis of plasma membrane proteins reveals regulatory mechanisms of plant innate immune responses. Plant Journal 51(5):931–940. https://doi.org/10.1111/j.1365-313X.2007.03192.x

Nühse, T. S., Stensballe, A., Jensen, O. N., and Peck, S. C. 2003. Large-scale analysis of in vivo phosphorylated membrane proteins by immobilized metal ion affinity chromatography and mass spectrometry. Molecular and Cellular Proteomics 2(11):1234–1243. https://doi.org/10.1074/mcp.T300006-MCP200

Olsson, A., Svennelid, F., Sommarin B. E. M., and Larsson C. 1998. A phosphothreonine residue at the c-terminal end of the plasma membrane H+-ATPase is protected by fusicoccin-induced 14-3-3 binding. Plant Physiology 118(2):551–555. https://doi.org/10.1104/pp.118.2.551

Palmgren, M. G. 2001. Plant plasma membrane H+-ATPases: powerhouses for nutrient uptake. Annual Review of Plant Biology 52:817–845. https://doi.org/10.1146/annurev.arplant.52.1.817

Pedersen, B. P., Buch-Pedersen, M. J., Morth, J. P., Palmgren, M. G., and Nissen, P. 2007. Crystal structure of the plasma membrane proton pump. Nature 450(7172):1111–1114. https://doi.org/10.1038/nature06417

Pedersen, C. N., Axelsen, K. B., Harper, J. F., and Palmgren, M. G. 2012. Evolution of plant P-type ATPases. Frontiers in Plant Science 3:31. https://doi.org/10.3389/fpls.2012.00031

Phillips, G. D., Preshaw, C., and Steer, M. W. 1988. Dictyosome vesicle production and plasma membrane turnover in auxin-stimulated outer epidermal cells of coleoptile segments from Avena sativa (L.). Protoplasma 145(1):59–65. https://doi.org/10.1007/BF01323257

Planes, M. D., Niñoles, R., Rubio, L., Bissoli, G., Bueso E., García-Sánchez, M. J., Alejandro, S., Gonzalez-Guzmán, M., Hedrich, R., Rodriguez, P. L., Fernández, J. A., and Serrano R. 2015. A mechanism of growth inhibition by abscisic acid in germinating seeds of Arabidopsis thaliana based on inhibition of plasma membrane H+-ATPase and decreased cytosolic pH, K+, and anions. Journal of Experimental Botany 66(3):813–825. https://doi.org/10.1093/jxb/eru442

Polevoi, V. 1986. Rol’ auksina v sistemakh regulyatsii u rastenii [Role of Auxin in Regulatory Systems of Plants]. Nauka Publishing, Leningrad.

Polevoi, V. V., Sinyutina, N. F., Salamatova, T. S., Inge-Vechtomova, N. I., Tankelyun, O. V., Sharova, E. I., and Shishova, M. F. 1996. Mechanism of auxin action: second messengers; pp. 223-231 in A. R. Smith, A. W. Berry, N. V. J. Harpham, I. E. Moshkov, G. V. Novikova, O. N. Kulaeva, and M. A. Hall (eds.), Plant hormone signal perception and transduction. Kluwer Academic Publishers, Dordrecht–
Boston–London. https://doi.org/10.1007/978-94-009-0131-5_30

Polevoi, V. V., and Salamatova T. A. 1977. Auxin, proton pump and cell trophics; pp. 209–216 in E. Marre, O. Ciferri (eds.), Regulation of cell membrane activities in plants. Elsevier, Amsterdam.

Portillo, F. 2000. Regulation of plasma membrane H+-ATPase in fungi and plants. Biochimica et Biophysica Acta (BBA)-Reviews on Biomembranes 1469(1):31–42. https://doi.org/10.1016/S0304-4157(99)00011-8

Quaite, E., Parker, R., and Steer, M. 1983. Plant cell extension: Structural implications for the origin of the plasma membrane. Plant, Cell and Environment 6(5):429–432. https://doi.org/10.1111/j.1365-3040.1983.tb01277.x

Ren, H. and Gray, W. M. 2015. SAUR proteins as effectors of hormonal and environmental signals in plant growth. Molecular Plant 8(8):1153–1164. https://doi.org/10.1016/j.molp.2015.05.003

Rubinstein, B. and Stern, A. I. 1986. Relationship of transplasmalemma redox activity to proton and solute transport by roots of Zea mays. Plant Physiology 80(4):805–811. https://doi.org/10.1104/pp.80.4.805

Ruck, A., Palme, K., Venis, M. A., Napier, R. M., and Felle, H. 1993. Patch-clamp analysis establishes a role for an auxin-binding protein in the auxin stimulation of plasma membrane current in Zea mays protoplasts. Plant Journal 4(1):41–46. https://doi.org/10.1046/j.1365-313X.1993.04010041.x

Rudashevskaya, E. L., Ye, J., Jensen, O. N., Fuglsang, A. T., and Palmgren, M. G. 2012. Phosphosite mapping of P-type plasma membrane H+-ATPase in homologous and heterologous environments. Journal of Biological Chemistry 287(7):4904–4913. https://doi.org/10.1074/jbc.M111.307264

Schenck, D., Christian, M., Jones, A., and Lüthen, H. 2010. Rapid auxin-induced cell expansion and gene expression: a four-decade-old question revisited. Plant Physiology 152(3):1183–1185. https://doi.org/10.1104/pp.109.149591

Shishova, M. and Lindberg, S. 1999. Auxin induces cytosol acidification in wheat leaf protoplasts depends on external concentration of Ca2+. Journal of Plant Physiology 155(2):190–196. https://doi.org/10.1016/S0176-1617(99)80006-6

Shishova, M. and Lindberg, S. 2004. Auxin induces an increase of Ca2+ concentration in the cytosol of wheat leaf protoplasts. Journal of Plant Physiology 161(8):937–945. https://doi.org/10.1016/j.jplph.2003.12.005

Shishova, M. and Lindberg, S. 2010. A new perspective on auxin perception. Journal of Plant Physiology 167(6):417–422. https://doi.org/10.1016/j.jplph.2009.12.014

Shishova, M. F., Inge-Vechtomova, N. I., Vykhvalov, K. A., Rudashevskaya, E. L., and Polevoi, V. V. 1998. Auxin-dependent transport of K+ and Ca2+ across the membrane of plasmalemma vesicles from coleoptile cells. Russian Journal of Plant Physiology 45(1):67–73.

Shishova, M. F., Lindberg, S. M., and Polevoi, V. V. 1999. Auxin activation of Ca2+ transport across the plasmalemma of plant cells. Russian Journal of Plant Physiology 46(5):626–633.

Shishova, M. F., Rudashevskaya, E. L., Inge-Vechtomova, N. I., Glinkina, M. V., Kirpichnikova, A. A., and Vykhvalov, K. A. 1999. Svoystva kationnykh kanalov plazmalemmy kletok koleoptiley kukuruzy, aktiviruemykh auksinom [Quality of maize coleoptile cell plasma membrane cation channels operated by auxin]. Biological Communications (3):36–43.

Shishova, M., Yemelyanov, V., Rudashevskaya, E., and Lindberg, S. 2007. A shift in sensitivity to auxin within development of maize seedlings. Journal of Plant Physiology 164(10):1323–1330. https://doi.org/10.1016/j.jplph.2006.09.005

Spartz, A. K., Lee, S. H., Wenger, J. P., Gonzalez, N., Itoh, H., Inzé, D., and Gray, W. M. 2012. The SAUR19 subfamily of SMALL AUXIN UP RNA genes promote cell expansion. Plant Journal 70(6):978–990. https://doi.org/10.1111/j.1365-313X.2012.04946.x

Spartz, A. K., Ren, H., Park, M. Y., Grandt, K. N., Lee, S. H., Murphy, A. S., Sussman, M. R., Overvoorde, P. J., and Gray, W. M. 2014. SAUR inhibition of PP2C-D phosphatases activates plasma membrane H+-ATPases to promote cell expansion in Arabidopsis. Plant Cell 26(5):2129–2142. https://doi.org/10.1105/tpc.114.126037

Sutter, J., Homann, U., and Thiel, G. 2000. Ca2+-stimulated exocytosis in maize coleoptile cells. Plant Cell 12(7):1127–1136. https://doi.org/10.1105/tpc.12.7.1127

Takahama, U., and Oniki, T. 1994. The association of ascorbate and ascorbate oxidase in the apoplast with IAA-enhanced elongation of epicotyls from Vigna angularis. Plant and Cell Physiology 35(2):257–266. https://doi.org/10.1093/oxfordjournals.pcp.a078591

Takahashi, K., Hayashi, K., and Kinoshita, T. 2012. Auxin activates the plasma membrane H+-ATPase by phosphorylation during hypocotyl elongation in Arabidopsis. Plant Physiology 159(2):632–641. https://doi.org/10.1104/pp.112.196428

Tian, H., Dieter, K. D., and Jones A. 1995. Auxin-binding protein 1 does not bind auxin within the endoplasmic reticulum despite this being the predominant subcellular location for this hormone receptor. Journal of Biological Chemistry 270(45):26962–26969. https://doi.org/10.1074/jbc.270.45.26962

Ueno, K., Kinoshita, T., Inoue, S., Emi, T., and Shimazaki, K. 2005. Biochemical characterization of plasma membrane H+-ATPase activation in guard cell protoplasts of Arabidopsis thaliana in response to blue light. Plant and Cell Physiology 46(6):955–963. https://doi.org/10.1093/pcp/pci104

Vanneste, S., and Friml, J. 2013. Calcium: The missing link in auxin action. Plants 2(4):650–675. https://doi.org/10.3390/plants2040650

Viotti, C., Luoni, L., Morandini, P., and De Michelis, M. I. 2005. Characterization of the interaction between the plasma membrane H+-ATPase of Arabidopsis thaliana and a novel interactor (PPI1). FEBS Journal 272(22):5864–5871. https://doi.org/10.1111/j.1742-4658.2005.04985.x

Xu, T., When, M., Nagawa, S., Fu, Y., Chen, J.-G., Wu, M.-J., Perrot-Rechenmann, K., Friml, J., Jones, A., and Yang, Z. 2011. Cell surface- and Rho GTPase-based auxin signaling controls cellular interdigitation in Arabidopsis. Cell 143(1):99–110. https://doi.org/10.1016/j.cell.2010.09.003

Yalovsky, S., Bloch, D., Sorek, N., and Kost, B. 2008. Regulation of membrane trafficking, cytoskeleton dynamics, and cell polarity by ROP/RAC GTPases. Plant Physiology 147(4):1527–1543. https://doi.org/10.1104/pp.108.122150
Published
2018-06-08
How to Cite
Kirpichnikova, A., Chen, T., Teplyakova, S., & Shishova, M. (2018). Proton pump and plant cell elongation. Biological Communications, 63(1), 32–42. https://doi.org/10.21638/spbu03.2018.105
Section
Review communications