How Does Auxin Enhance Cell Elongation? Roles of Auxin-Binding Proteins and Potassium Channels in Growth Control

Abstract

Elongation growth and a several other phenomena in plant development are controlled by the plant hormone auxin. A number of recent discoveries shed light on one of the classical problems of plant physiology: the perception of the auxin signal. Two types of auxin receptors are currently known: the AFB/TIR family of F box proteins and ABP1. ABP1 appears to control membrane transport processes (H⁺ secretion, osmotic adjustment) while the TIR/AFBs have a role in auxin-induced gene expression. Models are proposed to explain how membrane transport (e.g., K⁺ and H⁺ fluxes) can act as a cross-linker for the control of more complex auxin responses such as the classical stimulation of cell elongation.

Key words

Auxin - elongation growth - TIR1 - ABP1 - receptor - signal transduction.

References

• 1 Ballas N., Wong L. M., Theologis A.. Identification of the auxin responsive element, AuxRE, in the primary indoleacetic acid-inducible gene, PS-IAA4-5, of pea (Pisum sativum).  Journal of Molecular Biology. (1993);  233 580-596
• 2 Barbier-Brygoo H., Ephritikhine G., Klämbt D., Ghislain M., Guern J.. Functional evidence for an auxin receptor at the plasma membrane of tobacco mesophyll protoplasts.  Proceedings of the National Academy of Sciences of the USA. (1989);  86 891-895
• 3 Chen J. G., Ullah H., Young J. C., Sussman M. R., Jones A.. ABP1 is required for organized cell elongation and division in Arabidopsis embryogenesis.  Genes and Development. (2001);  15 902-911
• 4 Christian M., Steffens B., Schenck D., Lüthen H.. The diageotropica mutation of tomato disrupts a signalling chain using extracellular auxin binding protein 1 as a receptor.  Planta. (2003);  218 309-314
• 5 Christian M., Schenck D., Böttger M., Steffens B., Lüthen H.. New insight into auxin perception, signal transduction and transport.  Progress in Botany. (2006);  67 217-244
• 6 Claussen M., Lüthen H., Böttger M.. Inside or outside? Localization of the receptor relevant to auxin-induced growth.  Physiologia Plantarum. (1996);  98 861-867
• 7 Claussen M., Lüthen H., Blatt M., Böttger M.. Auxin-induced growth and its linkage to potassium channels.  Planta. (1997);  201 227-234
• 8 Coenen C., Bierfreund N., Lüthen H., Neuhaus G.. Developmental regulation of H⁺-ATPase dependent auxin responses in the diageotropica mutant of tomato (Lycopersicon esculentum).  Physiologia Plantarum. (2002);  114 461-471
• 9 Dela Fuente R. K., Leopold A. C.. Time course of the auxin stimulation of growth.  Plant Physiology. (1970);  46 186-189
• 10 Dharmasiri N., Dharmasiri S., Estelle M.. The F‐box protein TIR1 is an auxin receptor.  Nature. (2005 a);  435 441-445
• 11 Dharmasiri N., Dharmasiri S., Weijers D., Lechner E., Yamada M., Hobbie L., Ehrismann J. S., Jürgens G., Estelle M.. Plant development is regulated by a family of auxin receptor F box proteins.  Developmental Cell. (2005 b);  9 109-119
• 12 Diekmann W., Venis M. A., Robinson D. G.. Auxins induce clustering of the auxin binding protein at the surface of maize coleoptile protoplasts.  Proceedings of the National Academy of Sciences of the USA. (1995);  92 3425-3429
• 13 Dohrmann U., Hertel R., Kowalik H.. Properties of auxin binding sites in different subcellular fractions from maize coleoptiles.  Planta. (1978);  140 97-106
• 14 Ephritikhine G., Barbier-Brygoo H., Muller C. F., Guern J.. Auxin effect on the transmembrane potential difference of wild-type and mutant tobacco protoplasts exhibiting a different sensitivity to auxin.  Plant Physiology. (1987);  93 801-804
• 15 Frias I., Caldeira M. T., Perez-Castineira J. R., Navarro-Avino J. P., Culianez-Macia F. A., Kuppinger O., Stransky H., Pagés M., Hager A., Serrano R.. A major isoform of the plasma membrane H⁺-ATPase: Characterization and induction by auxin in coleoptiles.  Plant Cell. (1996);  8 1533-1544
• 40 Fuchs I., Philippar K., Hedrich R.. Ion channels meet auxin action.  Plant Biology. (2006);  8 353-359
• 16 Hager A., Menzel H., Krauss A.. Versuche und Hypothese zur Primärwirkung des Auxins beim Streckungswachstum.  Planta. (1971);  100 47-75
• 17 Hager A., Debus G., Edel H. G., Stransky H., Serrano R.. Auxin induces exocytosis and a rapid synthesis of a high turnover pool of plasma membrane H⁺-ATPase.  Planta. (1991);  185 527-537
• 18 Hertel R.. In vitro auxin binding to particulate fractions from corn coleoptiles.  Planta. (1972);  107 325-340
• 19 Hesse T., Feldwisch J., Balshüsemann D., Bauw G., Puype M., Vanderckove J., Löbler M., Klämbt D., Schell J., Palme K.. Molecular cloning and structural analysis of a gene from Zea mays L. coding for a putative receptor for the plant hormone auxin.  EMBO Journal. (1989);  8 2453-2461
• 20 Jones A. M., Im K.-H., Savka M. A., Wu M.-J., DeWitt N. G., Shillito R., Binns A. N.. Auxin-dependent cell expansion mediated by overexpressed auxin-binding protein 1.  Science. (1998);  282 1114-1117
• 21 Jones A. M., Herman E. M.. KDEL-containing auxin binding protein is secreted to the plasma membrane and cell wall.  Plant Physiology. (1993);  101 595-606
• 22 Keller C. P., Van Volkenburgh L.. Osmoregulation by oat coleoptile protoplasts.  Plant Physiology. (1996);  110 1007-1016
• 23 Kelly M., Bradford K. J.. Sensitivity of the diageotropica tomato mutant to auxin.  Plant Physiology. (1986);  82 713-717
• 24 Kepinski S., Leyser O.. The Arabidopsis F‐box protein TIR1 is an auxin receptor.  Nature. (2005);  435 446-451
• 25 Klämbt D.. A view about the function of auxin binding proteins at the plasma membranes.  Plant Molecular Biology. (1990);  14 1045-1050
• 26 Löbler M., Klämbt D.. Auxin-binding protein from coleoptile membranes of corn (Zea mays L.). I. Purification by immunological methods and characterization.  Journal of Biological Chemistry. (1985);  260 9848-9853
• 27 Lüthen H., Bigdon M., Böttger M.. Reexamination of the acid-growth theory of auxin action.  Plant Physiology. (1990);  93 931-939
• 28 MacDonald H.. Auxin perception and signal transduction.  Physiologia Plantarum. (1997);  100 423-430
• 29 Nebenführ A., White T. J., Lomax T.. The diageotropica mutation alters auxin induction of a subset of the Aux/IAA gene family in tomato.  Plant Molecular Biology. (2000);  44 73-84
• 30 Oh K. C., Hardeman K., Invanchenko M. G., Ellard-Ivey M., Nebenführ A., White T. J., Lomax T.. Fine mapping in tomato using microsynteny with the Arabidopsis genome: the diageotropica (Dgt) locus.  Genome Biology. (2002);  3 3-11
• 41 Oh K. C., Invanchenko M. G., White T. J., Lomax T. L.. The diageotropica gene of tomato encodes a cyclophilin: a novel player in auxin signalling.  Planta. (2006); 
• 31 Philippar K., Fuchs I., Lüthen H., Hoth S., Bauer C. S., Haga K., Thiel G., Ljung K., Sandberg G., Böttger M., Becker D., Hedrich R.. Auxin-induced K⁺ channel expression represents an essential step in coleoptile growth and gravitropism.  Proceedings of the National Academy of Sciences of the USA. (1999);  96 12186-12191
• 32 Ruge U.. Untersuchungen über den Einfluss des Heteroauxins auf das Streckungswachstum des Hypokotyls von Helianthus annuus. .  Zeitschrift für Botanik. (1937);  31 1-56
• 33 Rück A., Palme K., Venis M. A., Napier R. M., Felle H. H.. Patch clamp analysis establishes a role for an auxin binding protein in the auxin stimulation of a plasma membrane current in Zea mays protoplasts.  The Plant Journal. (1993);  4 41-46
• 34 Steffens B., Lüthen H.. New methods to analyse auxin-induced growth. II. The swelling reaction of protoplasts - a model system for the analysis of auxin signal transduction.  Plant Growth Regulation. (2000);  32 115-122
• 35 Steffens B., Feckler C., Palme K., Christian M., Böttger M., Lüthen H.. The auxin signal for protoplast swelling is perceived by extracellular ABP1.  The Plant Journal. (2001);  27 591-599
• 36 Thiel G., Weise R.. Auxin augments conductance of K⁺ inward rectifier in maize coleoptile protoplasts.  Planta. (1999);  208 38-45
• 37 Tode K., Lüthen H.. Fusicoccin - and IAA induced elongation growth share the same pattern of K+ dependence.  Journal of Experimental Botany. (2001);  52 251-255
• 38 Went F. W.. Wuchsstoff und Wachstum.  Recueil des Travaux Botaniques Néerlandais. (1928);  25 1-116
• 39 Woo E. J., Marshall J., Bauly J., Chen J. G., Venis M., Napier R. M., Pickersgill R. W.. Crystal structure of auxin binding protein 1 in complex with auxin.  EMBO Journal. (2002);  21 2877-2885

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