sign in sign up
<<
Home , Auxin

Review Article 353

Ion Channels Meet Auxin Action

I. Fuchs1, K. Philippar1, 2, and R. Hedrich1 1 Julius-von-Sachs-Institute, Molecular and Biophysics, Biocenter Würzburg University, Julius-von-Sachs-Platz 2, 97082 Würzburg, Germany 2 Present address: Department for 1, III, Ludwig-Maximilians-University Munich, Menzingerstraße 67, 80638 Munich, Germany

Received: November 17, 2005; Accepted: March 27, 2006

Abstract: The regulation of 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 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 , 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, , free IAA in the apical region was measured. This was most maize, thaliana. probably due to the release of IAA from its conjugated forms as an immediate response to the positional change of the seed- ling (Philippar et al., 1999). This pool of free auxin was redis- tributed 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 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, 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 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 (Went and Thimann, 1937). tion (Mulkey et al., 1981), which is consistent with the “Acid After the identification of IAA (-3-acetic acid) as this Growth Theory” established by Hager in 1971 (Hager et al., 1971). He proposed an acidification of the apoplast accom- plished 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 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. , 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 expres- sion 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 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 , 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 shown to be modu- half (Fuchs et al., 2003). As photostimulated seedlings display lated by the auxins IAA and 1-NAA (Marten et al., 1991; Lohse a much smaller bending angle than gravistimulated plants, and Hedrich, 1992; Blatt and Thiel, 1994). In maize coleoptile gravity seems to restrict further phototropic bending of the segments, auxin-induced growth strongly depends on the coleoptile. A clinostat equipped with blue LEDs (Blue Light Cy- availability of potassium ions in the bathing medium and their cler, BLC, see Fig.1), however, allowed simultaneous rotation uptake via potassium-selective ion channels: auxin-induced of the seedlings and illumination of the coleoptile tip uni- cell elongation could be very effectively inhibited by the use laterally (Fuchs et al., 2003). Thereby is uncou- of K+ channel blockers such as TEA+ or the removal of K+ ions pled from the blue light response. As expected, the bending an- from the external solution (Claussen et al., 1997). Based on gle of plants photostimulated on the BLC was comparable to these findings, the expression of K+ uptake channels in maize that of gravistimulated seedlings, but stronger bending could coleoptiles was studied (Philippar et al., 1999). While ZMK2 not be correlated to a more pronounced ZMK1 mRNA gradient (Zea mays K+ channel 2), the channel primarily localized in 90 min after the beginning of the experiment (Fuchs et al., vascular (Bauer et al., 2000; compare Deeken et al., 2003). However, auxin redistribution appeared to remain dif- 2000 and Deeken et al., 2002), was not regulated by auxins, ferential under varying gravity conditions. Interestingly, plants the transcription of ZMK1 (Zea mays K+ channel 1), the channel photostimulated on the BLC were characterized by a massive predominantly found in cortex and epidermal cells, was clear- rise in IAA in the shaded half of the coleoptile tip 60 min after ly induced in an auxin concentration-dependent manner (Phil- illumination onset, whereas this peak was missing in seedlings ippar et al., 1999; Bauer et al., 2000). Electrophysiological stud- exposed to unilateral blue light under normal gravity condi- ies revealed that ZMK1 is activated by extracellular acidifica- tions. Taking into account that the activation of ZMK1 tran- tion. In addition, the K+ channel density in ZMK1-expressing scription was detectable 45 – 60 min after the application of coleoptile protoplasts is significantly increased upon treat- auxin in earlier experiments (Philippar et al., 1999), it was hy- ment of the cells with 1-NAA. Regarding the localization of pothesized that the auxin peak in BLC-treated plants at 60 min ZMK1 in auxin-sensitive tissues, its transcriptional activation might lead to changes in ZMK1 transcription at a later time, not by IAA and the increase in channel activity in response to apo- previously investigated (Fuchs et al., 2003). By monitoring dif- plastic protons, it was tempting to speculate that ZMK1 might ferential ZMK1 expression for up to 4 h, it could indeed be Ion Channels Meet Auxin Action Plant Biology 8 (2006) 355

Fig.1 Blue Light Cycler (BLC): Experimental setup to uncouple pho- onset of clinostat rotation without illumination (right), or with simulta- totropism and the gravity response. Maize seedlings can be illuminated neous irradiation with blue light (left). (c) Magnified illustration of one with unilateral blue light during continuous rotation on a clinostat. (a) BLC slot, showing a single plant bending towards the light source. Side view. (b) Front view. Curvature of maize coleoptiles 24 h after the shown that, in seedlings photostimulated on the BLC, ZMK1 scription of auxin-regulated genes such as the PM-H+-ATPase transcription remains differential for at least 3 h, whereas a or ZMK1. In the long term, enhanced K+ uptake via ZMK1 into ZMK1 mRNA gradient is no longer visible in plants illuminated the cells of one coleoptile half very likely is a prerequisite for under normal gravity conditions (Fuchs et al., 2003). In our sustained differential growth and thus bending of the organ. working model, prolonged differential expression and thus en- hanced K+ uptake via ZMK1 is required for differential growth To confirm the importance of ZMK1-mediated K+ uptake for and stronger bending of BLC-treated plants. Therefore, the per- auxin-stimulated growth, Philippar et al. isolated ZMK1- ception of two different stimuli, blue light illumination and a knockout mutants. Thereby plants carrying Mutator transpos- change in the gravity vector, merges into a common signalling able element insertions inside the ZMK1 gene were identified pathway, leading to auxin redistribution, differential expres- (Philippar et al., 2006). Repeated backcrossing of the heterozy- sion of ZMK1, and differential cell elongation growth (Fig. 2). gous mutant plants, however, resulted in wild-type or hetero- zygous plants only, leading to the speculation that deletion of + Involvement of ZMK1 in Auxin-Induced this K channel might result in embryo or lethality. Cell Elongation Growth In fact, it was found that the expression of ZMK1 in wild-type embryos is massively induced around 40 days after pollina- Thus, the auxin regulation of a K+ channel gene provides a link tion, indicating that K+ uptake via this channel might also take between IAA redistribution and differential growth during part in processes underlying the development of the maize gravi- and phototropism. This led to the following sequence of embryo (Philippar et al., 2006). While maize seedlings are very events for auxin-induced cell elongation growth during gravi- well suited to study processes associated with tropistic bend- or phototropic bending of the maize coleoptile (Fig. 3): the ing of the coleoptile, genetic modification of maize plants raises direction of the incident light is perceived by the blue light some difficulties and is rather time-consuming, especially in photoreceptor PHOT1, which is equally distributed in the co- comparison to other model systems. Thus, maize might no lon- leoptile tip (Hager and Brich, 1993; Kaldenhoff and Iino, 1997; ger be a suitable system to study the involvement of K+ chan- Briggs et al., 2001). In contrast, it is less clear how the change nel action in auxin-induced growth in greater detail. Impor- in the gravity vector is perceived, but it is most probably medi- tantly, almost all studies on auxin signal transduction in the ated by the displacement of statoliths in the columella or past have been performed in , and here shoot endodermal tissues (Kiss et al., 1989; Kiss et al., 1997; re- most of the auxin-signalling mutants are available. viewed in Esmon et al., 2005). The perception of the two differ- ent stimuli, however, leads to the initiation of a common sig- Auxin-Regulated K+ Channels in Arabidopsis thaliana nalling pathway: Auxin is released from its conjugated forms in the shoot tip (Ljung et al., 2001) and translocated to one co- In Arabidopsis thaliana, however, the situation is more com- leoptile half by the action of auxin transporters of the PIN and plex than in maize, as several K+ channel genes are expressed AUX family (Swarup et al., 2001; Friml, 2003). High auxin con- in tissues that exhibit auxin-induced cell elongation growth. In centrations stimulate the activity of the PM-H+-ATPase, which the Arabidopsis , the organ homologous to grass co- results in the acidification of the apoplast and thus cell wall leoptiles in dicots, the mRNA of all known inward-rectifying loosening. Additionally, K+ channels already existing in the Shaker-type K+ channels, KAT1, KAT2, AKT1, AKT5, and AtKC1 plasma membrane might be activated by this decrease in ex- (Schachtman et al., 1992; Basset et al., 1995; Mäser et al., tracellular pH, enabling K+ uptake during the initial growth re- 2001; Pilot et al., 2001; Reintanz et al., 2002), was detected. In sponse, which might also be needed for charge compensation. stalks, where cell elongation growth can also be stimu- Furthermore, IAA is taken up into the cell and presumably per- lated by auxins, however, KAT1 (K+ uptake channel Arabidopsis ceived by the auxin receptor TIR1 or related F-Box proteins thaliana 1, see Schachtman et al., 1992) appeared to be the (Kepinski and Leyser, 2005; Dharmasiri et al., 2005a; Dharma- dominant K+ uptake channel (Philippar et al., 2004). Surpris- siri et al., 2005b). Binding of IAA to the receptor leads to the ingly, the expression of the ZMK1 ortholog in Arabidopsis thali- degradation of transcriptional repressors and thus to the tran- ana, AKT1 (Arabidopsis thaliana K+ transporter 1, Basset et al., 356 Plant Biology 8 (2006) I. Fuchs, K. Philippar, and R. Hedrich

Fig. 2 Two receptors – one signalling pathway. Signal perception in ZMK1, differential K+ uptake via this channel and thus bending of the gravi- or photostimulated coleoptiles is accomplished by the activation coleoptile. Graphs are adapted from Philippar et al. (1999) and Fuchs of different receptors, but merges into a common signalling pathway. et al. (2003). Auxin redistribution within the plant results in differential expression of

1995), was not induced by auxins. Similarly, the expression suggest a similar function in auxin-induced cell elongation of one of the ZMK1 homologues in rice, OsAKT1, was also un- growth. affected by the application of IAA. Rather than involvement in auxin action, OsAKT1, like AKT1, is involved in root K+ uptake Taking advantage of the availability of various knockout mu- from the soil and regulated in response to salt stress (Fuchs tants in Arabidopsis, the auxin-induced increase in KAT1 tran- et al., 2005). However, two other K+ channel genes in Arabidop- scripts was correlated with the abundance of the respective sis, KAT1 and KAT2 (a KAT1 homolog, see Pilot et al., 2001), protein (Philippar et al., 2004). In patch-clamp experiments were upregulated by the physiologically active auxins IAA and on protoplasts derived from hypocotyls of wild-type plants, 1-NAA in a concentration-dependent manner (Philippar et al., inward K+ currents were recorded upon hyperpolarization of 2004). Interestingly, the induction of KAT1 expression by 1- the plasma membrane. Surprisingly, similar results were ob- NAA was specific for organs that elongate in response to the tained using hypocotyl protoplasts of kat1 knockout plants application of auxin. In guard cells, however, where KAT1 also (kat1::En-1, Szyroki et al., 2001), although KAT1 transcripts represents the dominating K+ inward rectifier, its transcription were drastically reduced in the mutant (Philippar et al., was not induced upon auxin treatment (Philippar et al., 2004). 2004). This might be explained by the fact that Shaker K+ chan- This might indicate that the regulation of KAT1 expression by nels tend to form heterotetramers with other family members. auxins is associated with irreversible cell expansion during As the assembly of KAT1 and AKT1 has already been demon- elongation growth rather than transient volume changes dur- strated (Dreyer et al., 1997; Reintanz et al., 2002), it is very ing stomatal movement. It should be noted that KAT1, like likely that AKT1 might represent the dominating subunit of ZMK1, is activated upon acidification of the extracellullar heteromeric K+ uptake channels in the Arabidopsis hypocotyl. space (Hoth and Hedrich, 1999). This acid activation of both After the application of auxin, however, differences between channels and their expression in highly auxin-sensitive tissues protoplasts derived from wild type and kat1::En-1 could be Ion Channels Meet Auxin Action Plant Biology 8 (2006) 357

Fig. 3 Model to describe the involvement of K+ uptake via ZMK1 in lates cell wall loosening enzymes and ZMK1 channels already existing auxin-induced cell elongation growth. The perception of the gravi- or in the plasma membrane. Additionally, IAA signalling results in en- photostimulus by different receptors merges into a common signalling hanced transcription of both the PM-H+-ATPase and ZMK1. In the long pathway. Redistribution of IAA leads to the activation of the PM-H+- term, enhanced K+ uptake via ZMK1 leads to cell expansion and elon- ATPase and thus acidification of the extracellular space, which stimu- gation growth.

+ monitored (Philippar et al., 2004): The amplitude of K in cur- Conclusions rents in kat1::En-1 was reduced two-fold in comparison to wild type, which might reflect the fact that, upon auxin treat- In summary, the involvement of K+ channel activation in aux- ment, the proportion of KAT1 subunits within the K+ chan- in-induced cell elongation growth has been described in two nel complexes is increased in wild-type plants. Thus, auxin model plant systems. Furthermore, evidence has been provid- might regulate K+ uptake in Arabidopsis by shifting the subunit ed that the spatial regulation of K+ uptake via potassium-selec- + composition of the K in channel heteromers in favour of KAT1. tive channels might represent a prerequisite for differential To test the role of KAT1 for auxin-regulated growth, IAA-in- growth during tropistic bending. In the future, the regulation duced elongation of Arabidopsis hypocotyls in wild-type and of K+ channel action in response to an auxin stimulus will have kat1::En-1 plants was investigated (Philippar et al., 2004). Sur- to be investigated in more detail. For example, it remains to be prisingly, a significant difference in auxin-induced growth ki- elucidated if the transcriptional regulation of ZMK1 and KAT1/ netics of both genotypes was not detected, indicating that the KAT2 depends on a signalling pathway involving the action of role of KAT1 might be taken over by residual K+ channels. As TIR1 or related F-box proteins (Dharmasiri et al., 2005a; Dhar- already mentioned, several other K+ channel and carrier genes masiri et al., 2005b). The analysis of mutants defective in TIR1- (e.g., AtKUP2, Quintero and Blatt, 1997) are also expressed in associated signalling components identified in the future will the hypocotyl of Arabidopsis thaliana, probably compensating presumably help to shed light on this topic. Another question for the loss of KAT1 in the respective knockout. In this context, to be answered is if K+ channel regulation by IAA is strictly re- it is interesting to note that shy3-1 mutant plants defective in stricted to auxin-sensitive tissues such as the epidermal and AtKUP2 are characterized by reduced hypocotyl and cell cortical layers of maize coleoptiles or the epidermis of Arabi- expansion growth, pointing to the importance of K+ uptake dopsis hypocotyls and (Cleland, 1991; Peters et al., 1992; via this carrier for elongation growth (Elumalai et al., 2002). Swarup et al., 2005). Therefore, methods to detect K+ channel Further studies investigating the phenotype of double or triple transcript or protein abundance, even on a subcellular level, K+ transport mutants will have to be performed to reveal the will have to be developed. In this context, one could suspect individual contribution of each transport module to K+ uptake that, in response to a tropistic stimulus, K+ channel proteins during auxin-induced cell elongation growth in Arabidopsis. might be relocated within auxin-responding cells, as was dem- 358 Plant Biology 8 (2006) I. Fuchs, K. Philippar, and R. Hedrich

onstrated for the IAA efflux carrier PIN3 (Friml et al., 2002). Dharmasiri, N., Dharmasiri, S., Weijers, D., Lechner, E., Yamada, M., Here, it should be mentioned that an asymmetric intracellular Hobbie, L., Ehrismann, J. S., Jürgens, G., and Estelle, M. (2005b) distribution of a poplar K+ channel was recently discovered is regulated by a family of auxin receptor F (Arend et al., 2005). box proteins. Developmental Cell 9, 109– 119. Dietrich, P., Sanders, D., and Hedrich, R. (2001) The role of ion chan- Ion channels seem to play a role in the control of processes nels in light-dependent stomatal opening. Journal of Experimental such as cell cycle regulation, differential growth, stomatal Botany 52, 1959 – 1967. Dreyer, I., Antunes, S., Hoshi, T., Müller-Röber, B., Palme, K., Pongs, O., movement, plant-pathogen interactions, long-distance trans- Reintanz, B., and Hedrich, R. (1997) Plant K+ channel alpha-sub- port, nutrient uptake, and plant movement (see Dietrich et al., units assemble indiscriminately. Biophysical Journal 72, 2143 – 2001; Very and Sentenac, 2002; Becker and Hedrich, 2002; 2150. Very and Sentenac, 2003; Sano et al., 2006) and in the future Elumalai, R. P., Nagpal, P., and Reed, J. W. (2002) A mutation in the are expected to control many more cellular processes: “Ion Arabidopsis KT2/KUP2 potassium transporter gene affects shoot channels meet cell biology!” cell expansion. Plant Cell 14, 119– 131. Esmon, C. A., Pedmale, U. V., and Liscum, E. (2005) Plant tropisms: References providing the power of movement to a sessile organism. The Inter- national Journal of Developmental Biology 49, 665 –674. Arend, M., Stinzing, A., Wind, C., Langer, K., Latz, A., Ache, P., Fromm, Felle, H., Peters, W., and Palme, K. (1991) The electrical response of J., and Hedrich, R. (2005) Polar-localised poplar K+ channel capable maize to auxins. Biochimica et Biophysica Acta 1064, 199 –204. of controlling electrical properties of wood-forming cells. Planta Frias, I., Caldeira, M. T., Perez-Castineira, J. R., Navarro-Avino, J. P., Cu- 223, 140–148. lianez-Macia, F. A., Kuppinger, O., Stransky, H., Pages, M., Hager, A., Basset, M., Conejero, G., Lepetit, M., Fourcroy, P., and Sentenac, H. and Serrano, R. (1996) A major isoform of the maize plasma mem- (1995) Organization and expression of the gene coding for the po- brane H+-ATPase: characterization and induction by auxin in co- tassium transport system AKT1 of Arabidopsis thaliana. Plant Mo- leoptiles. Plant Cell 8, 1533– 1544. lecular Biology 29, 947– 958. Friml, J. (2003) Auxin transport – shaping the plant. Current Opinion Bauer, C. S., Hoth, S., Haga, K., Philippar, K., Aoki, N., and Hedrich, R. in Plant Biology 6, 7 –12. (2000) Differential expression and regulation of K+ channels in Friml, J., Wisniewska, J., Benkova, E., Mendgen, K., and Palme, K. the maize coleoptile: molecular and biophysical analysis of cells (2002) Lateral relocation of auxin efflux regulator PIN3 mediates isolated from cortex and vasculature. The Plant Journal 24, 139 – in Arabidopsis. Nature 415, 806 –809. 145. Fry, S. C., Smith, R. C., Renwick, K. F., Martin, D. J., Hodge, S. K., and Becker, D. and Hedrich, R. (2002) Channelling auxin action: modula- Matthews, K. J. (1992) Xyloglucan endotransglycosylase, a new tion of ion transport by indole-3-acetic acid. Plant Molecular Biol- wall-loosening enzyme activity from plants. Biochemical Journal ogy 49, 349 –356. 282, 821– 828. Blatt, M. R. and Thiel, G. (1994) K+ channels of stomatal guard cells: Fuchs, I., Philippar, K., Ljung, K., Sandberg, G., and Hedrich, R. (2003) bimodal control of the K+ inward-rectifier evoked by auxin. The Blue light regulates an auxin-induced K+ channel gene in the Plant Journal 5, 55 – 68. maize coleoptile. Proceedings of the National Academy of Sciences Briggs, W. R., Beck, C. F., Cashmore, A. R., Christie, J. M., Hughes, J., Ja- of the USA 100, 11795– 11800. rillo, J. A., Kagawa, T., Kanegae, H., Liscum, E., and Nagatani et al. Fuchs, I., Stölzle, S., Ivashikina, N., and Hedrich, R. (2005) Rice K+ up- (2001) The phototropin family of photoreceptors. Plant Cell 13, take channel OsAKT1 is sensitive to salt stress. Planta 221, 212– 993– 997. 221. Catala, C., Rose, J. K. C., and Bennett, A. B. (1997) Auxin regulation and Greenwood, M. S., Shaw, S., Hillman, J. R., Ritchie, A., and Wilkins, M. spatial localization of an endo-1,4-β-D-glucanase and a xyloglucan B. (1972) Identification of auxin from Zea coleoptile tips by mass endotransglycosylase in expanding tomato hypocotyls. The Plant spectrometry. Planta 108, 179 –183. Journal 12, 417– 426. Hager, A. (2003) Role of the plasma membrane H+-ATPase in auxin- Catala, C., Rose, J. K. C., and Bennett, A. B. (2000) Auxin-regulated induced elongation growth: historical and new aspects. Journal of genes encoding cell wall-modifying proteins are expressed during Plant Research 116, 483– 505. early tomato fruit growth. Plant Physiology 122, 527– 534. Hager, A. and Brich, M. (1993) Blue-light-induced phosphorylation of Cholodny, N. (1928) Beiträge zur hormonalen Theorie von Tropis- a plasma-membrane protein from phototropically sensitive tips of men. Planta 6, 118– 134. maize coleoptiles. Planta 189, 567–576. Claussen, M., Lüthen, H., Blatt, M., and Böttger, M. (1997) Auxin-in- Hager, A., Debus, G., Edel, H. G., Stransky, H., and Serrano, R. (1991) duced growth and its linkage to potassium channels. Planta 201, Auxin induces exocytosis and the rapid synthesis of a high-turn- 227– 234. over pool of plasma-membrane proton ATPase. Planta 185, 527– Cleland, R. E. (1991) The outer epidermis of Avena and maize coleop- 537. tiles is not a unique target for auxin in elongation growth. Planta Hager, A., Menzel, H., and Krauss, A. (1971) Versuche und Hypothese 186, 75 – 80. zur Primärwirkung des Auxins beim Streckungswachstum. Planta Cosgrove, D. J. (2000) Expansive growth of plant cell walls. Plant 100, 47 –75. Physiology and Biochemistry 38, 109– 124. Haschke, H. P. and Lüttge, U. (1973) β-Indolylessigsäure (IES)-abhän- Darwin, C. (1880) The Power of Movements in Plants. London: John giger K+-H+-Austauschmechanismus und Streckungswachstum Murray. bei Avena-Koleoptilen. Zeitschrift für Naturforschung 28C, 555 – Deeken, R., Geiger, D., Fromm, J., Koroleva, O., Ache, P., Langenfeld- 558. Heyser, R., Sauer, N., May, S., and Hedrich, R. (2002) Loss of the Haschke, H. P. and Lüttge, U. (1975) Stoichiometric correlation of ma- AKT2/3 potassium channel affects sugar loading into the late accumulation with auxin-dependent K+-H+ exchange and of Arabidopsis. Planta 216, 334– 344. growth in Avena coleoptile segments. Plant Physiology 56, 696 – Deeken, R., Sanders, C., Ache, P., and Hedrich, R. (2000) Developmen- 698. tal and light-dependent regulation of a phloem-localised K+ chan- Hoth, S. and Hedrich, R. (1999) Distinct molecular bases for pH sen- nel of Arabidopsis thaliana. The Plant Journal 23, 285 –290. sitivity of the guard cell K+ channels KST1 and KAT1. Journal of Bio- Dharmasiri, N., Dharmasiri, S., and Estelle, M. (2005a) The F-box pro- logical Chemistry 274, 11599 –11603. tein TIR1 is an auxin receptor. Nature 435, 441– 445. Ion Channels Meet Auxin Action Plant Biology 8 (2006) 359

Hutchison, K. W., Singer, P. B., McInnis, S., Diaz-Sala, C., and Green- Pilot, G., Lacombe, B., Gaymard, F., Cherel, I., Boucherez, J., Thibaud, J. wood, M. S. (1999) Expansins are conserved in conifers and ex- B., and Sentenac, H. (2001) Guard cell inward K+ channel activity in pressed in hypocotyls in response to exogenous auxin. Plant Phys- Arabidopsis involves expression of the twin channel subunits KAT1 iology 120, 827 –832. and KAT2. Journal of Biological Chemistry, 276, 3215 –3221. Iino, M. (1995) Gravitropism and phototropism of maize coleoptiles: Quintero,F. J. and Blatt, M. R. (1997) A new family of K+ transporters evaluation of the Cholodny-Went theory and through effects of from Arabidopsis that are conserved across phyla. FEBS Letters 415, auxin application and decapitation. Plant and Cell Physiology 36, 206– 211. 361 –367. Reintanz, B., Szyroki, A., Ivashikina, N., Ache, P., Godde, M., Becker, Iino, M. (1991) Mediation of tropisms by lateral translocation of en- D., Palme, K., and Hedrich, R. (2002) AtKC1, a silent Arabidopsis dogenous IAA in maize coleoptiles. Plant, Cell and Environment 14, potassium channel alpha-subunit modulates root hair K+ influx. 279 – 286. Proceedings of the National Academy of Sciences of the USA 99, Jahn, T., Johansson, F., Lüthen, H., Volkmann, D., and Larsson, C. 4079 –4084. (1996) Reinvestigation of auxin and fusicoccin stimulation of the Rose, J. K. C., Braam, J., Fry, S. C., and Nishitani, K. (2002) The XTH plasma-membrane H+-ATPase activity. Planta 199, 359– 365. family of enzymes involved in xyloglucan endotransglucosylation Kaldenhoff, R. and Iino, M. (1997) Restoration of phototropic respon- and endohydrolysis: current perspectives and a new unifying no- siveness in decapitated maize coleoptiles. Plant Physiology 114, menclature. Plant and Cell Physiology 43, 1421 –1435. 1267– 1272. Rück, A., Palme, K., Venis, M. A., Napier, R. M., and Felle, H. H. (1993) Kepinski, S. and Leyser, O. (2005) The Arabidopsis F-box protein TIR1 Patch-clamp analysis establishes a role for an auxin binding pro- is an auxin receptor. Nature 435, 446 –451. tein in the auxin stimulation of plasma membrane current in Zea Kiss, J. Z., Guisinger, M. M., Miller, A. J., and Stackhouse, K. S. (1997) mays protoplasts. The Plant Journal 4, 41 –46. Reduced gravitropism in hypocotyls of starch-deficient mutants Sano, T., Higaki, T., Handa, K., Kadota, Y., Kuchitsu, K., Hasezawa, S., of Arabidopsis. Plant and Cell Physiology 38, 518– 525. Hoffmann, A., Endter, J., Zimmermann, U., Hedrich, R., and Roitsch, Kiss, J. Z., Hertel, R., and Sack, F. D. (1989) Amyloplasts are necessary T. (2006) Calcium ions are involved in the delay of plant cell cycle for full gravitropic sensitivity in roots of Arabidopsis thaliana. Plan- progression by abiotic stresses. FEBS Letters 580, 597– 602. ta 177, 198 –206. Schachtman, D. P., Schroeder, J. I., Lucas, W. J., Anderson, J. A., and Ljung, K., Bhalerao, R. P., and Sandberg, G. (2001) Sites and homeo- Gaber, R. F. (1992) Expression of an inward-rectifying potassium static control of auxin biosynthesis in Arabidopsis during vegeta- channel by the Arabidopsis KAT1 cDNA. Science 258, 1654 – 1658. tive growth. The Plant Journal 28, 465 – 474. Swarup, R., Friml, J., Marchant, A., Ljung, K., Sandberg, G., Palme, K., Lohse, G. and Hedrich, R. (1992) Characterization of the plasma mem- and Bennett, M. (2001) Localization of the auxin permease AUX1 brane proton ATPase from Vicia faba guard cells: modulation by suggests two functionally distinct transport pathways extracellular factors and seasonal changes. Planta 188, 206– 214. operate in the Arabidopsis root apex. Genes and Development 15, Marten, I., Lohse, G., and Hedrich, R. (1991) Plant growth 2648– 2653. control voltage-dependent activity of anion channels in plasma Swarup, R., Kramer, E. M., Perry, P., Knox, K., Leyser, H. M. O., Haseloff, membrane of guard cells. Nature 353, 758 – 762. J., Beemster, G. T. S., Bhalerao, R., and Bennett, M. J. (2005) Root Mäser, P., Thomine, S., Schroeder, J. I., Ward, J. M., Hirschi, K., Sze, H., gravitropism requires cap and epidermal cells for Talke, I. N., Amtmann, A., Maathuis,F. J. M., Sanders, D., Harper, J. F., transport and response to a mobile auxin signal. Nature Cell Biol- Tchieu, J., Gribskov, M., Persans, M. W., Salt, D. E., Kim, S. A., and ogy 7, 1057 –1065. Guerinot, M. L. (2001) Phylogenetic relationships within cation Szyroki, A., Ivashikina, N., Dietrich, P., Roelfsema, M. R. G., Ache, P., transporter families of Arabidopsis. Plant Physiology 126, 1646 – Reintanz, B., Deeken, R., Godde, M., Felle, H., Steinmeyer, R., Palme, 1667. K., and Hedrich, R. (2001) KAT1 is not essential for stomatal open- Mulkey, T. J., Kuzmanoff, K. M., and Evans, M. L. (1981) Correlations ing. Proceedings of the National Academy of Sciences of the USA between proton-efflux patterns and growth patterns during geo- 98, 2917–2921. tropism and phototropism in maize and sunflower. Planta 152, Thiel, G. and Weise, R. (1999) Auxin augments conductance of K+ in- 239– 241. ward rectifier in maize coleoptile protoplasts. Planta 208, 38 –45. Nelles, A. (1977) Short-term effects of plant hormones on membrane Very, A. A. and Sentenac, H. (2002) Cation channels in the Arabidopsis potential and membrane permeability of dwarf maize coleoptile plasma membrane. Trends in Plant Science 7, 168 –175.

cells (Zea mays L. d1) in comparison with growth responses. Planta Very, A. A. and Sentenac, H. (2003) Molecular Mechanisms and Reg- 137, 293 –298. ulation of K+ Transport in higher Plants. Annual Review of Plant Bi- Parker, K. E. and Briggs, W. R. (1990) Transport of IAA during gravi- ology 54, 575 –603. tropism in intact maize coleoptiles. Plant Physiology 94, 1763 – Went, F. W. (1928) Wuchsstoff und Wachstum. Receuil des Travaux 1769. Botaniques Neerlandais 25, 1 –116. Peters, W. S., Richter, U., and Felle, H. H. (1992) Auxin-induced H+- Went, F. W. and Thimann, K. V. (1937) Phytohormones. New York: pump stimulation does not depend on the presence of epidermal Macmillan. cells in corn coleoptiles. Planta 186, 313 –316. Philippar, K., Büchsenschütz, K., Edwards, D., Löffler, J., Lüthen, H., Kranz, E., Edwards, K. J., and Hedrich, R. (2006) The auxin-induced R. Hedrich K+ channel gene ZMK1 in maize functions in coleoptile growth and Julius-von-Sachs-Institute is required for embryo development. Plant Molecular Biology, in Molecular Plant Physiology and Biophysics press. Biocenter Würzburg University Philippar, K., Fuchs, I., Lüthen, H., Hoth, S., Bauer, C., Haga, K., Thiel, G., Julius-von-Sachs-Platz 2 Ljung, K., Sandberg, G., Böttger, M., Becker, D., and Hedrich, R. 97082 Würzburg (1999). Auxin-induced K+ channel expression represents an essen- Germany tial step in coleoptile growth and gravitropism. Proceedings of the National Academy of Sciences of the USA 96, 12186– 12191. E-mail: [email protected] Philippar, K., Ivashikina, N., Ache, P., Christian, M., Lüthen, H., Palme, K., and Hedrich, R. (2004) Auxin activates KAT1 and KAT2, two K+- Guest Editor: R. Reski channel genes expressed in seedlings of Arabidopsis thaliana. The Plant Journal 37, 815 –827.