Review
A new perspective on auxin perception

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Abstract

An important question in modern plant biology concerns the mechanisms of auxin perception. Despite the recently discovered soluble receptor, the F-box protein TIR1, there is no doubt that another type of signal perception exists, and is linked to the plasma membrane. Two models for the receptor have been suggested: either the receptor includes a protein kinase, or it is coupled with a G-protein. We propose a third model, acting through Ca2+-channels in the plasma membrane. The model is based on the revealed rapid auxin-induced reactions, including changes in the membrane potential, shifts in cytosol concentration of Ca2+ and H+ and modulation of cell sensitivity to hormones by the external Ca2+ concentration. Detailed inhibitor analysis with both living cells and isolated plasma membranes show that auxin might directly stimulate Ca2+ transport through the plasma membrane. A hypothetical scheme of auxin perception at the plasma membrane is suggested together with further transduction events. In addition, comparative analyses of auxin and serotonin perceptions are provided.

Introduction

For more than 100 years the most intriguing question in plant physiology has been how a small indolic molecule like auxin (indole-3-acetic acid, IAA) might trigger such enormous variety in physiological responses. According to recent knowledge, such broad spectral activity might correlate with changes in the number and properties of auxin receptors. These proteins are responsible for recognition of the hormone and the initiation of further signal transduction chains, resulting in a specific physiological response. Thus, one of the main properties of the auxin receptor is its capability to bind auxin. An investigation of auxin-binding sites in plant cells started almost 30 years ago (Hertel et al., 1972) and showed heterogeneity of these sites in affinity and localization (reviewed in Batt and Venis, 1976; Batt et al., 1976; Dohrmann et al., 1978; Venis and Napier, 1995). In brief, the pool of plant cell auxin-binding proteins (ABPs) consists of two groups: soluble and membrane-bound proteins.

Section snippets

Soluble auxin-binding proteins

Early biochemical investigations identified a number of auxin-binding soluble proteins such as 1,3-glucanase (MacDonald et al., 1991), ß-glucosidase (Campos et al., 1992), glutathione S-transferase (Bilang et al., 1993) and superoxide dismutase (Feldwisch et al., 1994). Two soluble ABPs with a relatively low affinity for IAA were purified and reported to stimulate RNA synthesis in isolated nuclei (Kikuchi et al., 1989). Later, it was shown that one of these proteins bound RNA polymerase II and

Soluble auxin receptors

In contrast to all of these proteins, a 57 kDa auxin-binding protein (ABP 57) mediates auxin-dependent stimulation of the plasma membrane H+-ATPase through binding with an autoinhibiting C-terminal enzyme domain (Kim et al., 1998, Kim et al., 2000). The ABP57 is suspected to fulfill the role of an intracellular auxin receptor, which rapidly enhances the activity of the H+-pump, known to be involved in an auxin-induced cell enlargement. Unfortunately, we still know little about the genes encoding

Membrane-bound auxin receptors. The role of ABP1

Membrane-bound sites were initially subdivided into three classes: site I, localized in the endoplasmic reticulum (ER), site II, localized in the tonoplast/Golgi and site III, localized in the plasma membrane (Hertel et al., 1972; Batt and Venis 1976; Batt et al., 1976; Ray et al., 1977; Dohrmann et al., 1978). Site III was suggested to fulfill the role of an IAA transporter (Lomax et al., 1985, Lomax et al., 1995; Morris, 2000). There are 3 types of auxin transporters in the plasma membrane:

Models of plasma membrane auxin receptors considering ABP1 as an associated domain

The amino acid sequence analysis revealed that ABP1 did not form a hydrophobic transmembrane domain (Hesse et al., 1989; Tillmann et al., 1989). Nevertheless, the rapid auxin-induced reactions, such as a shift in intensity of ion transport, indicate that ABP1 has activity at the plasma membrane. This coincides with earlier findings showing a short-lived pool of ABP1 at the cell surface (Diekmann et al., 1995). It was suggested that ABP1 might be coupled with a transmembrane (docking) protein (

Alternative model for the plasma membrane auxin receptor

Several authors have shown that exogenous auxin led to a complicated (usually oscillating) change of membrane potential, starting with a depolarization and then changing to a hyperpolarisation (Stahlberg and Polevoi, 1978; Güring et al., 1979; Felle et al., 1986; Keller and von Volkenburgh, 1996). The depolarization coincided in time with auxin-triggered Ca2+ uptake by coleoptile segments from incubation medium (Shishova et al., 1999). The intensity of the uptake strongly depended on the Ca2+

Perception of serotonin in animal cells

Serotonin (5-hydroxytryptamine, 5-HT) controls a variety of physiological functions in the central and peripheral nervous systems. Serotonin action is mediated by various 5-HT receptor subtypes, which might be divided into seven main classes (5-HT1 – 5-HT7, Hoyer et al., 2002). Except for the 5-HT3 all represent G-protein coupled receptors. The 5-HT3 is a ligand-gated Ca2+-channel and belongs to a family of Cys-loop receptors, including receptors for major neurotransmitters such as

Summary and perspectives

The suggested model of the PM receptor complex is in line with data on further transduction events (Fig. 1). Addition of auxin triggers an increase in Ca2+ permeability of the plasma membrane in the presence of high (1 mM) apoplastic concentrations of this ion. This will transiently inhibit activity of the PM H+-ATPase resulting in a relatively intensive acidification. Accumulation of protons will later activate the enzyme (supposed by Polevoi et al., 1996), and/or in parallel cause a Ca2+

Acknowledgements

We particularly want to thank, for the last time, Prof. V. Polevoi, St. Petersburg State University, Russia, who died in 2001. He gave the initial prompting of our work with auxin and followed it with encouragement throughout 12 years of investigation. We are very thankful to Prof. R. Napier for valuable discussion and comments and to Dr. V. Yemelyanov for help with manuscript preparation. Financial support was provided by Swedish Institute, KSLA, Wallenberg Foundation, Russian foundation for

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