Ion Channels Meet Auxin Action

Review Article 353 Ion Channels Meet Auxin Action I. Fuchs1, K. Philippar1, 2, and R. Hedrich1 1 Julius-von-Sachs-Institute, Molecular Plant Physiology and Biophysics, Biocenter Würzburg University, Julius-von-Sachs-Platz 2, 97082 Würzburg, Germany 2 Present address: Department for Biology 1, Botany III, Ludwig-Maximilians-University Munich, Menzingerstraße 67, 80638 Munich, Germany Received: November 17, 2005; Accepted: March 27, 2006 Abstract: The regulation of cell division and elongation in plants growth-promoting substance (Greenwood et al., 1972), this is accomplished by the action of different phytohormones. Aux- assumption known as the “Cholodny-Went Hypothesis” was in as one of these growth regulators is known to stimulate cell confirmed by Parker and Briggs (1990) and Iino (1991). elongation growth in the aerial parts of the plant. Here, auxin en- hances cell enlargement by increasing the extensibility of the cell The kinetics of auxin redistribution, however, varies in re- wall and by facilitating the uptake of osmolytes such as potassi- sponse to different tropistic stimuli. Moritoshi Iino demon- um ions into the cell. Starting in the late 1990s, the auxin regula- strated that, while in photostimulated plants endogenous aux- tion of ion channels mediating K+ import into the cell has been in is redistributed only in the very tip, IAA is laterally translo- studied in great detail. In this article we will focus on the mole- cated along the length of the entire coleoptile in gravistimulat- cular mechanisms underlying the modulation of K+ transport by ed plants (Iino, 1995). Measuring free endogenous IAA in gravi- auxin and present a model to explain how the regulation of K+ or photostimulated maize coleoptiles, Fuchs et al. (2003) and channels is involved in auxin-induced cell elongation growth. Philippar et al. (1999) confirmed these findings. Already 5 min after the onset of gravistimulation, a significant increase in Key words: Auxin, K+ channel, elongation growth, tropisms, free IAA in the apical region was measured. This was most maize, Arabidopsis thaliana. probably due to the release of IAA from its conjugated forms as an immediate response to the positional change of the seedling (Philippar et al., 1999). This pool of free auxin was redistributed in the coleoptile tip as early as 15 min after the be- Auxin History ginning of gravistimulation and this relocation further spread over the entire length of the coleoptile during the course of the More than one hundred years ago Charles Darwin and his son experiment. In photostimulated coleoptiles, however, a signif- Francis initiated studies on auxin-regulated growth processes icant auxin gradient between the growing shaded half and the (Darwin, 1880). Investigating photostimulated grass coleop- growth-restricted illuminated half could not be detected until tiles, they hypothesized that “some influence” coming from 60 min after the onset of blue light irradiation (Fuchs et al., the coleoptile tip moves downwards and causes phototropic 2003). As expected, a pronounced translocation of free auxin bending of the seedlings. Different concentrations of this sig- was not observed in the basal part of the seedling. This trans- nalling component in the opposing flanks of the coleoptile location was found only in the coleoptile tip. were proposed to cause differential cell elongation growth and thus curvature. Almost fifty years later, Frits Went and Auxin-Dependent Membrane Polarization, Cell Wall Nicolai Cholodny discovered that this phytohormone, now Acidification, and Wall Loosening termed auxin (derived from the greek word “auxein”, meaning “to grow”), is transported to the shaded flank of the photostim- Up to now, it is not fully understood how the auxin gradient as ulated coleoptiles, where high auxin concentrations stimulate a signal in tropistically stimulated plants is converted into the cell elongation and thus cause bending of the seedling towards bending response. One of the first steps to be identified was the light source (Cholodny, 1928; Went,1928). Hence, differen- the change in apoplastic pH which is associated with the redis- tial growth and bending of both gravi- or photostimulated tribution of auxin. The concentration of protons is increased in grass coleoptiles was identified as a consequence of the un- the apoplast of the fast-growing half of gravi- or photostimu- equal distribution of the “growth stimulating substance” in lated coleoptiles, characterized by an elevated IAA concentra- the opposing flanks of the organ (Went and Thimann, 1937). tion (Mulkey et al., 1981), which is consistent with the “Acid After the identification of IAA (indole-3-acetic acid) as this Growth Theory” established by Hager in 1971 (Hager et al., 1971). He proposed an acidification of the apoplast accomplished by the enhanced activity of the PM-H+-ATPase as a pre- Plant Biol. 8 (2006): 353 –359 requisite for cell elongation in response to increased auxin con- © Georg Thieme Verlag KG Stuttgart · New York centrations. In fact, in auxin-sensitive Vicia faba guard cells, DOI 10.1055/s-2006-924121 treatment with the synthetic auxin 2,4-D activates the H+- ISSN 1435-8603 ATPase and thus causes the plasma membrane to hyperpolar- 354 Plant Biology 8 (2006) I. Fuchs, K. Philippar, and R. Hedrich ize (Lohse and Hedrich, 1992). In maize coleoptiles IAA treat- play a role during auxin-induced growth. Interestingly, the in- ment does not only seem to increase the proton pump activity crease in growth rate of coleoptile segments treated with the but also the density of the respective protein in the plasma synthetic auxin 1-NAA was accompanied by a rise in ZMK1 membrane (Hager et al., 1991; Felle et al., 1991; Rück et al., mRNA. This transcriptional induction was delayed by approxi- 1993; Frias et al., 1996). It should be noted that Jahn et al. mately 15 min in relation to the growth rate, but otherwise (1996), for example, could not confirm this finding, a contro- almost superimposed it (see “Channeling auxin action” by versy which might result from the fact that not all isoforms of Becker and Hedrich, 2002 for review). In patch clamp studies, the PM-H+-ATPase are induced by auxins. Thus, the induction K+ channel activation can already be seen 10 min after auxin of MHA2 might have been masked by unregulated ATPases stimulation (Philippar et al., 1999; Thiel and Weise, 1999). This (see also Hager, 2003). strongly suggests the involvement of K+ uptake via ZMK1 in cell elongation. One possible explanation for the abovemen- In the context of his theory, Hager also proposed that the de- tioned delay might be that the initial rise in growth rate is crease in apoplastic pH leads to the activation of cell wall-loos- due to acidification of the apoplast and subsequent cell wall ening enzymes. Expansins, catalytic acid-activated proteins loosening. K+ uptake via ZMK1 might thus be required for sus- which loosen bonds between cellulose and hemicellulose fi- tained growth, characterized by the need to take up osmotical- brils in the cell wall, are potential candidates to perform this ly active substances. task (reviewed by Cosgrove, 2000). Interestingly, the expression of some expansins is also regulated by auxins (Hutchison K+ Channel Expression Follows Auxin Redistribution et al., 1999; Catala et al., 2000). Additionally, XTHs (xyloglucan During Gravi- and Phototropism endotransglucosylases/hydrolases, Rose et al., 2002), another class of acid-activated enzymes (Fry et al., 1992), may enhance As mentioned above, differential cell elongation growth regu- the plasticity of the cell wall by regulating the xyloglucan turn- lated by auxin gradients is the basic principle for tropistic over. It is interesting to note that one XTH expressed in tomato bending of plant organs. Assuming that ZMK1 also participates hypocotyls, LeEXT is transcriptionally induced by the synthetic in these processes, ZMK1 expression was found to follow aux- auxin 2,4-D as well (Catala et al., 1997). in redistribution in response to a gravitropic stimulus: ZMK1 transcripts gradually decreased in the upper half of gravistim- Auxin Activation of K+ Channels ulated maize coleoptiles, which is characterized by a depletion of IAA, whereas the amount of ZMK1 mRNA in the lower, fast- Apart from cell wall loosening, the uptake of osmolytes pro- growing half remained constant (Philippar et al., 1999). This vides a basic requirement for cell elongation growth. More- differential expression of the K+ channel gene led to 6 – 7-times over, to balance the charge of the secreted protons, cations higher ZMK1 mRNA levels in the auxin-enriched lower coleop- have to be imported into the cell, a task easily fulfilled by the tile half 90 min after the onset of gravistimulation. In photo- uptake of potassium ions, the most prevalent cations in plants. stimulated maize seedlings, ZMK1 expression also followed It has been known since the 1970s that auxin-induced H+ the translocation of endogenous auxin, but the difference in pumping is accompanied by the uptake of K+ ions in grass ZMK1 transcripts in the opposing flanks was not as pro- coleoptiles (Haschke and Lüttge, 1973, 1975; Nelles, 1977). In nounced as seen with the gravity response: 90 min after the guard cells, where auxin does not only promote elongation onset of blue light illumination, the ZMK1 mRNA content was growth but also stimulates the activity of the proton pump, K+ only 2 – 3-times higher in the faster-growing shaded coleoptile and anion channel activity have also been

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