Polar Auxin Transport and Asymmetric Auxin Distribution

In all multicellular organisms extensive communication is required between cells and tissues in order to coordinate growth and development. Both plants and animals have signaling chemicals, traditionally termed hormones that mediate short- and long-distance communication. The first phytohormone to be discovered was auxin, a substance that has since been implicated in an increasingly wide variety of developmental processes. It has emerged from decades of studies that a unique property of auxin - its directional movement between cells (polar auxin transport) - is a crucial process in auxin biology. In this report, we will first review the key events in the history of auxin research and then explore the current concepts and latest findings of the mechanisms of polar auxin transport and the resulting asymmetric auxin distribution. The history of auxin began in the late 19th century when Charles and Francis Darwin were studying the phototropic responses of canary grass coleoptiles. They demonstrated the existence of an influence which moved from the tip of the coleoptile to the region below where it controlled bending (Darwin and Darwin, 1881). In fact, this was the first experimental demonstration of a plant signaling molecule and its intercellular movement. Some years later, in 1913, Boysen-Jensen was able to pass this influence through an agar block, thus confirming the chemical nature of this growth-promoting substance. Another important and visionary experiment was performed by Frits Went in 1926. He demonstrated that agar blocks soaked with the growth-promoting substance, when placed off-center on the decapitated coleoptiles, were sufficient to promote their bending away from the side that the block was sitting (Went, 1926; Cholodny, 1927; Went and Thimann, 1937; Went, 1974). Since this substance promoted coleoptile elongation, it was named auxin (from the Greek word auxein, which means: to increase, to grow) (Kogl and Haagen-Smit, 1931). It was later identified as indole-3-acetic acid (IAA) (reviewed by Thimann, 1977). While IAA seems to be the most physiologically important form of auxin, other natural forms exist, such as indole-3-butyric acid (IBA) and 4-chloroindole-3-acetic acid (4-Cl-IAA). There are also commonly known and useful synthetic auxins, such as 1-naphthaleneacetic acid (1-NAA) or 2,4-dichlorophenoxy-acetic acid (2,4-D). The natural and synthetic auxins differ in their effective concentrations, metabolic stability and transport properties (reviewed by Normanly et al., 2004; Woodward and Bartel, 2005). These early studies not only identified different auxins as regulators of plant growth but also highlighted the significance of polar auxin transport and indicated that asymmetric auxin distribution may be important for the tropic growth responses. The identification of substances that can inhibit auxin flow (Katekar and Geissler, 1977; Jacobs and Rubery, 1988) established that cellular auxin efflux is crucial for auxin transport and provided tools for further studies into the physiological importance of this process. Studies using these inhibitors combined with auxin transport experiments led, in the middle 1970s, to the formulation of the chemiosmotic hypothesis, which proposed a mechanism by which auxin could move from cell to cell. It postulated that auxin is transported into and out of the cell through the action of specific carrier proteins (Rubery and Sheldrake, 1974; Raven, 1975). Importantly, it also proposed that the strictly controlled directionality of auxin flow may be a result of the asymmetric cellular localization of auxin efflux carriers. The chemiosmotic hypothesis gained significant support from genetic studies in Arabidopsis thaliana that led to the identification and characterization of molecular components of auxin influx (AUX1/LAX family) and auxin efflux (PIN family) (Bennett et al., 1996; Luschnig et al., 1998; Galweiler et al., 1998), as well as the identification of several PGP proteins from the ABC transporter superfamily, which are also involved in transport of auxin across the plasma membrane (Petrasek et al., 2006; Geisler et al., 2005). Many of the molecular components of polar auxin transport (PAT), in particular PIN proteins, show asymmetric localization at the cell membrane within auxin transport-competent cells as predicted by the chemiosmotic hypothesis. Progress into the characterization of the molecular components of auxin response and signaling (Ulmasov et al., 1997; Gray et al., 2001; Dharmasiri et al., 2005: Kepinski and Leyser, 2005) also allowed the presence of auxin to be indirectly observed in plant cells and tissues. By comparing indirect and direct auxin measurements, these studies identified local, asymmetric auxin distribution (auxin gradients), which are the result of PAT, and which underpin most of the auxin-mediated developmental processes (for overview see Tanaka et al., 2006). These findings also highlighted the morphogenic properties of auxin and stirred the old debate on the morphogen versus hormone characteristics of auxin (Friml, 2003; Bhalearo and Bennett, 2003). Even though most of the information about the molecular mechanism of PAT and recent physiological insights came from studies in Arabidopsis, research conducted in other plant organisms (e.g. rice, maize, tobacco, Brassica) or suspension cultured cells (e.g. tobacco BY-2 cells), as well as the use of heterologous cell systems (e.g. yeast or human HeLa cells), also greatly contributed to our knowledge about auxin transport, often supporting and complementing studies from Arabidopsis.