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First published online July 17, 2003; 10.1104/pp.103.022129 Plant Physiology 132:2256-2266 (2003) © 2003 American Society of Plant Biologists Aluminum-Induced Gene Expression and Protein Localization of a Cell Wall-Associated Receptor Kinase in Arabidopsis1 ek BalukaMolecular Cytology Core Facility, Molecular Biology Program, 2 Tucker Hall, University of Missouri, Columbia, Missouri 65211–7400 (M.S.); Research Institute for Bioresources, Okayama University, Chuo 2–20–1, Kurashiki 710–0046, Japan (B.E., H.O., H.M.); Department of Biology, San Francisco State University, San Francisco, California 94132 (Z.-H.H., H.T.); and Department of Plant Cell Biology, Rheinische Friedrich-Wilhelms University of Bonn, Kirchalle 1, D–53115 Bonn, Germany (F.B., D.V.)
Here, we report the aluminum (Al)-induced organ-specific expression of a WAK1 (cell wall-associated receptor kinase 1) gene and cell type-specific localization of WAK proteins in Arabidopsis. WAK1-specific reverse transcriptase-polymerase chain reaction analysis revealed an Al-induced WAK1 gene expression in roots. Short- and long-term analysis of gene expression in root fractions showed a typical "on" and "off" pattern with a first peak at 3 h of Al exposure followed by a sharp decline at 6 h and a complete disappearance after 9 h of Al exposure, suggesting the WAK1 is a further representative of Al-induced early genes. In shoots, upon root Al exposure, an increased but stable WAK1 expression was observed. Using confocal microscopy, we visualized Al-induced closure of leaf stomata, consistent with previous suggestions that the Al stress primarily experienced in roots associated with the transfer of root-shoot signals. Elevated levels of WAK protein in root cells were observed through western blots after 6 h of Al exposure, indicating a lag time between the Al-induced WAK transcription and translation. WAK proteins are localized abundantly to peripheries of cortex cells within the elongation zone of the root apex. In these root cells, disintegration of cortical microtubules was observed after Al treatment but not after the Al analog lanthanum treatments. Tip-growing control root hairs, stem stomata, and leaf stomatal pores are characterized with high amounts of WAKs, suggesting WAKs are accumulating at plasma membrane domains, which suffer from mechanical stress and lack dense arrays of supporting cortical microtubules. Further, transgenic plants overexpressing WAK1 showed an enhanced Al tolerance in terms of root growth when compared with the wild-type plants, making the WAK1 one of the important candidates for plant defense against Al toxicity.
In animal and human cells, extracellular matrix (ECM) proteins such as vitronectin and fibronectin are directly linked to transmembrane receptors known as integrins that are associated with components of the cytoskeleton within the cytosol (Miyamoto et al., 1995  ; Maniotis et al.,
1997; Schoenwaelder and
Burridge, 1999; Critchley,
2000). Such structural continuity facilitates transfer of external
signals from the cell periphery to the cytoplasm, where growth and defense
mechanisms in animal cells are orchestrated
(Ingber, 1991;
Schwartz et al., 1995;
Dedhar and Hannigan, 1996).
Obviously, plant cells are also equipped with an analogous structural
continuum, but individual players, especially the plasma membrane
(PM)-associated connectors, have yet to be identified
(Wyatt and Carpita, 1993;
Fowler and Quatrano, 1997;
Miller et al., 1997;
Horst et al., 1999;
Kohorn, 2000). Integrins and
their ECM-binding partners have been proposed repeatedly, but plant proteins
reactive to heterologous integrin antibodies often do not localize to the PM
(e.g. Lynch et al., 1998). In
addition, sequence identities of some potential candidates are too low to be
defined as plant homologs of vitronectins
(Zhu et al., 1994) or
integrins (Nagpal and Quatrano,
1999). In fact, a plant vitronectin-like protein turned out to be
more than 93% identical to elongation factor-1
(Zhu et al., 1994). More
importantly, recent completion of sequencing of the Arabidopsis genome
revealed that this plant, like the budding yeast (Saccharomyces
cerevisiae) genome, lacks an integrin homolog. The absence of integrins
in both yeast and plant may be explained because their ECMs are built largely
from unique polysaccharide polymers, which are not related to the
proteinaceous polymers of animal ECMs. Moreover, plant cell wall proteins are
typically unrelated to proteins of animal ECMs
(Bolwell, 1993;
Showalter, 1993;
Nothnagel, 1997;
Cassab, 1998;
Majewska-Sawka and Nothnagel,
2000). Alternative to animal integrins, plants may utilize unique
adhesive proteins. Wall-associated kinases (WAKs), pectins, and
arabinogalactan proteins have been proposed recently as key players in the
adhesion of the PM to the cell wall (e.g.
Miller et al., 1997;
Kohorn, 2000;
Majewska-Sawka and Nothnagel,
2000; Park et al.,
2000;  amaj et al.,
2000; Anderson et al.,
2001; Wagner and Kohorn,
2001).
Although plant homologs of integrins, vitronectins, and fibronectins might
still be identified in the future, several plant receptor protein kinases
characterized during the last few years (for review, see
Harmon et al., 1996
It has been repeatedly shown that aluminum (Al) induces expression of
several genes, which share a high degree of similarity to proteins induced by
pathogen attack, wounding, or oxidative stresses (e.g.
Cruz-Ortega and Ownby, 1993
Short-Term Al Impacts on Root Growth To better understand the early response of root growth to Al, a highly sensitive short-term root growth analysis was carried out. The root growth inhibition by Al became prominent after 6 h of Al treatment. From 9 h onwards, the Al-treated plants showed about 50% of growth inhibition when compared with the control plants (Fig. 1).
To characterize the WAK1 gene expression in response to Al stress, reverse transcriptase (RT)-PCR was performed using the total RNAs extracted from plants that were exposed to 100 µM Al for various time intervals (0–9 h). The relative mRNA level of the WAK1 gene was determined by PCR with several different cycles (20, 25, and 30 for the short-term treatments and 25, 30, and 35 cycles for the long-term treatments) to determine optimal number of cycles to estimate the amount of PCR products. In the short-term Al treatment, WAK1 expression gradually increased over time and reached the maximum level after 1 h of Al treatment (Fig. 2A).
The different cycles of PCR for the detection of long-term Al treatment showed similar results. The relative expression induction (Fig. 2C) of WAK1 gene in the long-term treatment (0, 3, 6, and 9 h) was calculated from the result of 30 cycles in Figure 2B. Maximum accumulation of the WAK1 transcripts occurs 3 h after Al treatment (Fig. 2C), and a moderate decrease was observed at 6 h of treatment. An apparent gene induction can also be detected in the top regions of the Al-treated Arabidopsis seedlings at 3 h of Al treatment, and this elevated level of WAK1 transcripts remains unchanged at 6 and 9 h of Al treatment.
The WAK1 expression induction by Al treatment was investigated
with western-blot analysis. The polyclonal WAK antibody recognized a single
band (at approximately 69 kD) in whole-plant protein fractions in Arabidopsis
seedlings (ecotypes Landsberg and Columbia;
Fig. 3A). However, it must be
presumed that the WAK1 antibody recognizes all five WAK isoforms because this
antibody is directed against epitopes within the cytoplasmic kinase domain,
which is 90% identical among five WAKs of Arabidopsis
(He et al., 1998
The effect of Al treatment of WAK protein expression and distribution was analyzed by indirect immunofluorescence technique coupled with confocal microscopy. We have processed intact whole mounts of seedlings for immunofluorescence labeling of WAKs in the leaf stomatal guard cells (Fig. 4). WAK proteins are localized heavily in guard cells (Fig. 4A). Almost all leaf stomata were closed after 9 h of Al treatments (Fig. 4B) compared with their respective controls (Fig. 4A). To determine whether this response is Al-specific, parallel experiments performed with lanthanum, an Al analog failed to induce this phenomenon (Fig. 4C). There were no clear differences in stomatal apertures observed from Al treatments in less than the 9-h period (data not shown).
Because cortical microtubules (MTs) play a crucial role in cell elongation and because Al has been shown to disrupt these processes, we have analyzed this in the context of WAK protein expression/localization. Double labeling of WAKs and MTs enabled us simultaneous acquisition and analysis of both WAKs localization and MT arrangement in cells of intact Al-treated root apices. In the root apices of control plants, WAKs are localized in the form of fine cytoplasmic "spots" starting from the basal part of the meristematic zone (Fig. 5A). We imaged cells in individual root growth zones separately. In control plants, there was low WAK expression at the very tip of the root apex (Fig. 5A). The WAK expression in cells of the elongation zone of the same root apex was noticeable (Fig. 5A'). This feature does not alter dramatically after 3 h of Al treatment (data not shown), but after 6 h of Al treatment, the WAK expression increased dramatically in cells of both the meristematic and elongation zones (Fig. 5, B and B'). After 9 h of Al treatment, WAK signal dropped and became diffused as comparable with the 3-h level (data not shown). There was no such tendency found in the root apices treated with lanthanum, particularly 6 h after treatments (Fig. 5, C and C').
After 9 h of Al treatment, MTs were completely depolymerized (Fig. 6C) compared with their respective controls (Fig. 6A) and the WAK signals emanating as continuous lining along the PM in the basal parts of elongation region (Fig. 6E), whereas WAK-positive cytoplasmic particles also were clearly evident in the mature root zones (Fig. 6G). Neither the complete depolymerization of cortical MTs (Fig. 6B) nor the lining of the PM with WAKs at the basal parts of elongation zone (Fig. 6D) or mature root zone (Fig. 6F) were observed in roots subjected to lanthanum, suggesting the induction of WAK specifically to Al toxicity.
To test whether WAK1 actually plays a physiological role in Arabidopsis Al response, transgenic plants overexpressing WAK1 were generated. In the transgenic plants, an ectopic copy of the WAK1 gene was fused to the constitutive 35S promoter. The construct was transformed into Arabidopsis wild-type (WT) plants (ecotype Columbia), and 30 transgenic lines were produced. Western-blot analysis confirmed that there was a severalfold increased level of WAK1 protein in one-third of the generated WAK1 overexpression lines (data not shown). Figure 7B shows severalfold higher level of WAK1 protein in one of the overexpression lines (WAK10X) when compared with WT. For the Al response test, 5-d-old seedlings of both the WT and WAK10X were transferred to Murashige and Skoog or Murashige and Skoog with Al media, and their root growth was monitored by measuring the positions of the root tips every 24 h. Seedlings of both the WT and the WAK10X had similar root lengths (10 mm) before the transfer of seedlings to a new set of plates with or without Al. One hundred micromolar Al had a noticeable effect on the root growth of both the WT and WAK1-overexpressing plants. The WAK1-overexpressing plants showed a 3-fold increase in growth in the presence of Al (Fig. 7, A and C) compared with the growth of WT plants in the presence of Al.
Over 20 Al-induced genes have been isolated from wheat (Triticum aestivum), tobacco (Nicotiana tabacum), and yeast cells so far. Some of them, such as pEARLI1 and pEARLI8 genes, show an early response to Al stress manifested within the first few hours (Richards et al., 1998 ). In
this paper, we demonstrate that WAK1 is a further representative of
early genes induced by Al in Arabidopsis. Our results with the WAK1
expression pattern and the site of WAK1 protein localization (elongation
zone), together with WAK1 overexpression studies, strongly suggest a
functional role of WAK1 in the Al tolerance. Also, our RT-PCR results
suggest that the mRNA level of the WAK1 gene is extremely low in
roots. The rapid Al-mediated up-regulation identifies WAK1 gene as a
good candidate for genes rendering tolerance toward the Al toxicity in
Arabidopsis. WAK1 has been shown to play a role in abiotic stress; therefore,
we have focused on this expression to Al toxicity because there are several
isoforms of WAKs present in plants, and we cannot rule out the fact that other
isoforms may also play a role in Al response.
The WAK1 gene has been reported to be a member of the
pathogenesis-related (PR) genes in Arabidopsis
(He et al., 1998
WAK1 expression induced by Al proceeds in both root and
aboveground organs without any considerable lag time, although the Al
treatment was applied only to the root region. Therefore, the WAK1
induction in aboveground organs could not be caused by a direct Al effect but
must result from Al-induced signals originating from roots. Larsen et al.
(1996
Although the mechanism of WAK1 involvement in Al tolerance is not
clear, our northern-blot results suggests that the Al-induced WAK1
gene expression is part of the early response to the Al stress. Furthermore,
the cytoplasmic kinase activity of these PM-associated receptor kinases (He et
al., 1996
Al is well known to alter properties of biological membranes, which appear
as the major target of Al toxicity
(Wagatsuma et al., 1995
On the other hand, an intriguing possibility remains that cytoplasmic
kinase domains can be cleaved off from WAKs and then participate in the
putative cytoplasmic Al response pathways. In fact, a significant portion of
the WAK fluorescence is cytoplasmic, indicating that the protein kinase part
of WAK, against which the polyclonal antibody used in our study has been
raised (He et al., 1996
We found that PM-associated WAKs accumulate in large amounts specifically
at such subcellular domains that suffer from internal mechanical stresses and
that lack dense supporting arrays of cortical MTs underlying the PM. Here, we
document this feature for extending tips of root hairs and stomatal pores. It
may not be just a coincidence that these cell periphery domains also
accumulate callose/pectin and are depleted in cellulosic microfibrils (e.g.
Kumarasinghe and Nutman, 1977
PM-associated callose synthesis is the alternative to cellulose synthesis
(Jacob and Northcote, 1985
Plant Material and Growth Conditions
The Arabidopsis ecotype Landsberg erecta (Ler-0) seeds, sterilized
using commercial bleach, were incubated at 4°C for 4 d and grown for 7 d
on the nylon membrane described previously
(Ezaki et al., 2000
Seedlings with 2- to 3-cm root length were removed from the nylon membrane and subjected to one-sixth Murashige and Skoog containing 100 µM Al or lanthanum (chloride salts) for 9 h (approximately 60 seedlings per 120 mL of medium). Some portions of Al-treated plants were removed from Al medium after designated time points (0, 15, 30, 45, 60, and 240 min for short-term Al treatment and after every 3 h until 12 h for long-term Al treatment), washed profusely in distilled water, and stored at -80°C until extraction of total RNA or proteins. Root growth rate was measured at 3-h intervals during the 12-h Al treatment (100 µM). For root growth measurements (for Fig. 1), six to 10 plants were removed from the treatment solution, and after determining the initial root lengths, the root growth was measured at 3-h intervals using an Olympus stereomicroscope (SZ 60, Olympus Company Ltd., Tokyo) under 20x magnification.
For root growth analyses of the WAK1 overexpression transgenic
lines, seeds were surface sterilized, cold treated for more than 48 h, and
germinated in plates containing a growth medium as described above without Al.
After 5 d, seedlings were transferred to the same medium that contains Al, and
the plates were placed vertically in a growth chamber at 22°C with 14 h of
light (200 µmol m-2 s-1). Root growth was measured by
marking the positions of the root tips every 24 h. Root length measurements
were made as described previously (Lally
et al., 2001
Total RNA was extracted from root and shoot (stem and leaves) regions
separately or from whole plants after Al treatments using an extraction
reagent (TRIZOL Reagent, GIBCO-BRL, Rockville, MD). First strand cDNA was
synthesized in a 25-µL reaction containing approximately 2 µg of total
RNA using Superscript Pre-amplification System for First Strand cDNA Synthesis
(Life Technologies, Inc., Rockville, MD) and oligo(dT) 12-18 as a primer.
Using the synthesized first strand cDNA as a template and two primers derived
from the WAK1 gene (5'-CTACATCAGGTCGCATCAAGC-3' and
5'-TCATAGT-GGTGGTATCTAAGCGG-3') as primers, PCR with different
cycles (25, 30, and 35 cycles) was performed. The PCR products were applied to
1% (w/v) agarose gel electrophoresis and stained with ethidium bromide. The
strength of fluorescent signal derived from ethidium bromide in each lane was
determined using the National Institutes of Health Image analysis program
(version 1.57). By using the two primers derived from the
After experimental treatments, the whole Arabidopsis plants were handled as
described elsewhere (Harper et al.,
1996 A set of plants incubated only with secondary antibodies served as negative controls. The double-labeled whole seedlings including leaves were treated with 0.01% (w/v) Toluidine Blue to diminish the natural autofluorescence of plant tissues. The labeled plants were mounted in 0.2 M Tris (pH 8.5) and 10% (v/v) glycerol containing Mowiol (Calbiochem, La Jolla, CA) to avoid fluorescence fading.
The images of MTs from roots and leaf stomatal guard cells were obtained using the 488-nm excitation line (long pass 560) of an argon laser, and the tetramethylshortamine-isothiocyanate fluorescence of WAKs was imaged using the 543-nm excitation line of the He-Ne laser in a Zeiss microscope (Axioplan II) coupled with the confocal module (LSM 510, Carl Zeiss, Oberkochen, Germany). The images obtained from different distances from tip positions of the root surface and shoots/leaves from at least 10 replicate plants in a treatment, using the Ph3-Plan-Neofluar 100x oil immersion (1.3 numerital aperture) objective were documented systematically. The root surface confocal images were the overlay of seven to 11 optical sections (1.0 µm thick) of roots from the surface. In the case of leaves, stem, and root hairs, the top 5 to 10 µm was optically sectioned at 0.55-µm intervals, and the composite images were displayed. By using the reuse mode of the LSM software, uniform scanning parameters such as pinhole, amplifier offset, and gain were used for both MTs and WAK images and between treatments to facilitate intensity comparisons. All images stored permanently in the computer hard disc in RGB format were organized using Adobe Photoshop 7.0 (Adobe Systems Inc., San Jose, CA).
Total proteins for tissue-specific western blots were extracted according
to the method of He et al.
(1996 Total protein (60 µg) was fractionated by 12.5% (w/v) SDS-PAGE and electroblotted onto polyvinylidene difluoride membrane using a semidry blotting apparatus at 2 mA constant current cm-1 of membrane for 2 h at 4°C, blocked with 2% (v/v) blocking reagent (Amersham) in PBS (10 mM phosphate buffer [pH 7.4] containing 138 mM NaCl and 2.7 mM KCl) for 1 h, and then incubated with WAK polyclonal antibody at a dilution of 1:500 (v/v) in PBS for 1 h at room temperature. After three washes in PBS (15 min each), the membrane was incubated with a goat anti-rabbit IgG secondary antibody conjugated to alkaline phosphatase (Bio-Rad Laboratories, Hercules, CA) at a dilution of 1:3,000 (v/v) in PBS for 1 h at room temperature. After further washing (3 x 15 min) in PBS, the antigen-antibody complex was visualized by a chemiluminescence system according to the manufacturer's protocol (Amersham).
We thank Drs. Tobias I. Baskin and Jia Li (University of Missouri, Columbia) for their critical reading and valuable suggestions regarding the presentation and organization of results. Received February 16, 2003; returned for revision March 30, 2003; accepted May 12, 2003.
1 This work was supported by the Program for the Promotion of Basic Research Activities in Innovative Biosciences; by the Ministry of Agriculture, Forests, and Fisheries, Japan (to H.M.); by the Japan Society for the Promotion of Science (postdoctoral fellowship to M.S.); and by the National Science Foundation (grant no. MCB–9985135 to Z.-H.H.).  * Corresponding author; e-mail hmatsumo{at}rib.okayamau.ac.jp; fax 81–86–434–1249.
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-tubulin gene
(Knight et al., 1999
