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First published online March 2, 2007; 10.1104/pp.106.094052 Plant Physiology 143:1695-1704 (2007) © 2007 American Society of Plant Biologists Actin Is Involved in Auxin-Dependent Patterning1Institute of Botany 1, University of Karlsruhe, D–76128 Karlsruhe, Germany
Polar transport of auxin has been identified as a central element of pattern formation. The polarity of auxin transport is linked to the cycling of pin-formed proteins, a process that is related to actomyosin-dependent vesicle traffic. To get insight into the role of actin for auxin transport, we used patterned cell division to monitor the polarity of auxin fluxes. We show that cell division in the tobacco (Nicotiana tabacum L. cv Bright-Yellow 2) cell line is partially synchronized and that this synchrony can be perturbed by inhibition of auxin transport by 1-N-naphthylphthalamic acid. To address the role of actin in this synchrony, we induced a bundled configuration of actin by overexpressing mouse talin. The bundling of actin impairs the synchrony of cell division and increases the sensitivity to 1-N-naphthylphthalamic acid. Addition of the polarly transported auxins indole-3-acetic acid and 1-naphthyl acetic acid (but not 2,4-dichlorophenoxyacetic acid) restored both the normal organization of actin and the synchrony of cell division. This study suggests that auxin controls its own transport by changing the state of actin filaments.
The promotion of growth and signaling from both developmental programs and environmental stimuli are often mediated by auxin, one of the major plant hormones. In addition, auxin is involved in directional cues fundamental to patterning (for review, see Berleth and Sachs, 2001  ). Classical examples for auxin-dependent patterning have been the formation of leaf veins (Mattsson et al., 1999), the positioning of meristems (Reinhard et al., 2000), and the organization of vascular tissue (Sachs, 2000).
The cellular base of auxin-dependent patterning is related to the establishment of a directional flow. This polar transport of auxin is a cell-to-cell process that has been described in a modified chemiosmotic model for auxin transport (for review, see Lomax et al., 1995
This implies that patterning is brought about by communication between cells that exchange morphogenetic signals in a defined direction. In other words, patterning is driven by cell polarity. Therefore, synchrony and coordination between neighboring cells are of extreme importance for the development of a functional tissue (Sachs, 1993
The self amplification of cell polarity by a polar auxin flow has been linked with directional intracellular traffic that contains positive feedback loops in combination with lateral inhibition, resulting in an ordered pattern (for review, see Nick, 2006
Several experiments demonstrated the central role of basipetal auxin transport in mediating this directionality, mainly by means of the polarized activity of auxin efflux carriers (for review, see Morris, 2000
When plant samples are treated with brefeldin A (BFA) that selectively blocks secretory pathways from endosomes to the plasma membrane, the plasma membrane-localized PIN1 protein is trapped in intracellular compartments (Steinmann et al., 1999
A link between actin and auxin signaling has also been proposed from studies on auxin-dependent cell growth in Graminean coleoptiles. In this model, an auxin-dependent reorganization of actin filaments into fine cortical strands could be shown to correlate with the auxin response of growth (Waller et al., 2002
The actin cytoskeleton has also been implicated in regulating gravitropism, because interruption of intact actin filaments by the actin depolymerization drug latrunculin B enhances the gravitropic responses in different plant species (Hou et al., 2004
In general, an intact actin cytoskeleton is required for functional auxin responses. Because the organization of actin in turn depends on auxin, this constitutes a self-amplification loop between auxin signaling and actin filaments (for review, see Nick, 2006
In a previous work, we used patterned cell division in tobacco (Nicotiana tabacum) L. cv Virginia Bright Italia 0 (VBI-0) cells to monitor the polarity of auxin fluxes (Campanoni et al., 2003
The use of the model tobacco BY-2 has generated a wealth of data on the role of phytohormones during the plant cell cycle (Nagata et al., 1992
The BY-2 cell line grows in simple files that exhibit basic characteristics of pattern formation, such as clear axis and polarity of cell division and growth. Therefore, this system is well suited to study spatial aspects of cell division. In fact, it could be shown that high concentrations of NPA perturb the axiality of cell division. For instance, the formation of preprophase bands was abnormal, leading to disoriented, oblique cell plates and malformed cells (Dhonukshe et al., 2005 To test this prediction, we used a transgenic BY-2 cell line stably expressing a fusion between the yellow fluorescent protein (YFP) and the actin-binding domain of mT. In this cell line, the actin filaments are constitutively bundled, and the synchrony of cell division is impaired in such a way that the pattern of cell division is affected. When we added polar transportable auxins (but not auxin per se), both a normal organization of actin and the synchrony of cell division could be restored. We therefore conclude that actin is not only responsive to changes in the cellular content of auxin but also that the organization of actin filaments is crucial for auxin transport. This indicates a regulatory mechanism by which auxin controls its own transport through changing the organization of actin filaments.
Cell Division within Cell Files of BY-2 Is Synchronized by a NPA-Sensitive Signal To assess cell division patterns, we first had to define the onset of the stationary phase. We therefore followed the time course of cell division in nontransformed BY-2 cells and in BY-2 cells overexpressing YFP-mT. Although cell division activity in the YFP-mT line was delayed by about 0.5 to 1 d and reduced in amplitude, the temporal pattern was very similar, and cell density approached a plateau from 4 d after subcultivation (Fig. 1A ). We therefore constructed at this time point frequency distributions over the cell number per individual file.
Under standard cultivation conditions, the frequency distribution of nontransformed BY-2 cells exhibited characteristic peaks of frequency for files composed of two, four, and six cells (Fig. 1B). Similar distributions were observed throughout the entire exponential phase (data not shown). Thus, files with even cell numbers are more frequent than files with uneven cell numbers. In the next step, we asked whether this characteristic pattern was related to auxin transport. Therefore, BY-2 cells were inoculated in presence of 3 or 12 µM NPA, an inhibitor of polar auxin transport. The concentrations were chosen such that neither polarity nor axiality of cell files nor their viability were affected (data not shown). What was affected under these conditions was the distribution of cell division (Fig. 1, C and D). Treatment with these low concentrations of NPA progressively equalized the frequencies of files with even and uneven cell numbers, especially for files with a higher number of cells. It should be noted that, at 3 µM NPA, cell division (Fig. 1, F1 and F2) was only slightly reduced and cell elongation (Fig. 1G) was not affected at all. From 12 µM NPA, the inhibition of cell division became evident (Fig. 1, F1 and F2), and cell elongation increased progressively (Fig. 1G1). However, for a high concentration (30 µM) of NPA, the upper two frequency peaks disappeared (Fig. 1E), and files with more than four cells became very rare. Under these conditions, we observed a strong inhibition of cell division (Fig. 1, F1 and F2) and a significant stimulation of cell elongation (Fig. 1G1) that were accompanied by a loss of file polarity and axiality. Although the cells significantly increased in length, they exhibited localized swellings, resulting in irregular, bulbous cell shapes (Fig. 1G2). In addition, the difference between the more pointed terminal cells of a file and the more isodiametric cells in the center of a file vanished progressively. We tested whether the loss of synchrony was limited to NPA or whether it could be induced by other inhibitors of polar auxin flow. We therefore tested the effect of 12 µM 2,3,5-triiodobenzoic acid (TIBA) and observed that, similar to NPA, the synchrony of cell division was lost such that the difference in frequency between even and uneven cell numbers disappeared (Fig. 5A). To test whether the observed loss of synchrony might be caused by a precocious and randomized disintegration of cell files, we calculated the mean number of cells per file as indicator. For 3 µM of NPA, where synchrony was already conspicuously affected (Fig. 1C), this indicator was almost identical with that of untreated control cells (3.91 versus 4.09). Thus, the reduced synchrony is not due to premature disintegration. We also recorded the possible influence of aberrant cell divisions (oblique or longitudinal). These were occasionally observed, but at such a rare frequency that there was no statistically measurable effect on the frequency distributions (data not shown).
Because NPA blocks auxin efflux and causes accumulation of auxin within cells, the actual effect might be an accumulation of auxin due to reduced efflux. If this idea is correct, one would predict that a mild treatment with NPA combined with addition of low concentrations of the polar transportable auxin indole-3-acetic acid (IAA) in nontransformed cells should phenocopy the effect of a high concentration of NPA. We therefore tested what happened when nontransformed cells were treated by a combination of a low (3 µM) concentration of NPA with a low (2 µM) concentration of IAA. We observed that this resulted in a conspicuous loss of division synchrony mimicking the effect of a high (12 µM) concentration of NPA (Fig. 5B). These data show that, in this cell line, the pattern of cell division depends on polar auxin flow within the cell file (despite the overall presence of 0.9 µM of the artificial auxin 2,4-dichlorophenoxyacetic acid [2,4-D] in the medium). The synergistic effect of low concentrations of NPA with low concentrations of IAA indicates that it is the intracellular accumulation of IAA that is responsible for the reduced synchrony in response to the phytotropin NPA.
To better understand the role of actin in auxin-dependent patterning, we searched for a situation where actin filaments were constitutively bundled. For this purpose, we generated a transgenic BY-2 cell line stably transformed with a fusion between YFP and the actin-binding domain of mT under control of a 35S promoter. We wanted to test whether the excess of YFP-mT fusion would cause a constitutive bundling of actin filaments. If so, it should be possible, by means of the YFP-mT line, to manipulate auxin-dependent patterning through the altered organization of actin in this cell line. Therefore, we compared the arrangement of actin filaments in nontransformed control cells with cells overexpressing YFP-mT (Figs. 2 and 3 ). The actin cytoskeleton was visualized either in nontransformed BY-2 cells by the rhodamine-phalloidin staining method or, in the case of the BY-2 YFP-mT line, observed directly in vivo.
To confirm that YFP-mT binds to and visualizes actin filaments, BY-2 cells overexpressing the fusion protein were also costained with rhodamine-phalloidin. Patterns of yellow YFP-fluorescence and red rhodamine-phalloidin fluorescence emitted from double-labeled BY-2 cells were essentially identical (Fig. 2), showing that YFP-mT binds to the entire actin cytoskeleton in a specific manner. The nontransformed BY-2 cells displayed a fine network of transversely oriented actin filaments in the cortical region (Fig. 3A). Prominent fine actin filaments were also visible around the nucleus and radially oriented in transvacuolar strands (Fig. 3B). In contrast, actin was heavily bundled in cells overexpressing YFP-mT both in the cortical (Fig. 3E) and in the perinuclear regions (Fig. 3F). These observations demonstrate that the overexpression of the actin-binding domain of mT indeed induced a strong reorganization of the actin cytoskeleton.
With exception of a small delay and a somewhat reduced amplitude of the division response, the global temporal pattern of cell division in the YFP-mT line was comparable to that in the nontransformed BY-2 cell line (Fig. 1A). However, the synchrony of cell division was affected in the YFP-mT line (Fig. 4A ). The characteristic oscillatory behavior typical for the nontransformed control is hardly detectable. In other words, the difference in the incidence of files with even and uneven cell numbers is strongly reduced in YFP-mT cells. This difference was persistent when the selective pressure on the cell line was relieved by omitting hygromycin from the medium, suggesting that it is an effect of the transgene and not an effect of the selection pressure. The average number of cells per file as indicator for a possible precocious disintegration of files did not reveal significant differences to the nontransformed wild type (3.93 versus 4.09, respectively). Thus, the reduced synchrony in the YFP-mT line is not due to a premature disintegration of cell files. We also scored for the possible influence of aberrant cell divisions but were not able to detect any statistically measurable effect on synchrony.
We further investigated how the pattern of cell division responded to treatment with NPA. Similar to the nontransformed BY-2 cell line, the frequency peaks for higher cell numbers disappeared progressively (Fig. 4, B and C). Generally, the YFP-mT cell line appeared to be affected more readily compared to the nontransformed cell line. Already, for 12 µM, NPA files with more than two cells had become very rare (Fig. 4C), whereas in the nontransformed cell line, a higher concentration (30 µM NPA) was required to cause a similar effect (Fig. 1E). Conversely, the effect of 3 µM NPA in the YFP-mT cell line was comparable to that observed in the nontransformed cell line upon addition of 12 µM NPA. Moreover, cell division was more impaired (Fig. 1, F1 and F2), and cell elongation was more elevated (Fig. 1G1) at 12 µM NPA in the YFP-mT cell line compared to the nontransformed cell line. Because viability at 30 µM NPA was strongly reduced in the YFP-mT cell line (in contrast to the nontransformed cell line), it was not possible to measure cell division responses for the transgenic line (data not shown). In summary, already low concentrations of NPA caused effects in the YFP-mT cell line that were observed in the nontransformed cell line only for higher concentrations of this inhibitor. In other words, the YFP-mT line is, in sensu strictu, more sensitive to NPA compared to the nontransformed BY-2 cell line. These data show that the synchrony of cell division is already a priori strongly deteriorated compared to the nontransformed cell line. This is accompanied by an elevated sensitivity of cell division to NPA. Thus, the constitutive bundling of actin filaments in the YFP-mT line was accompanied by impaired synchrony in auxin-dependent patterning.
If the observed correlation between constitutively bundled actin and impaired synchrony of cell division is the manifestation of a causal relationship, we would predict that synchrony should be restored when the microfilament bundles are replaced by a configuration with finer, detached actin filaments. To test this prediction, we tried to generate detached microfilament strands by addition of supplementary auxins. The BY-2 cells overexpressing YFP-talin were cultivated either upon addition of the auxins IAA or 1-naphthyl acetic acid (NAA) that are both polarly transported or the same concentration of 2,4-D, an auxin that, at least in BY-2 cells, was not a good substrate for the efflux carrier responsible for polar auxin flow (Delbarre et al., 1996 The presence of IAA leads to a debundling of actin both in the cortical region and around the nucleus. In contrast to the massive actin bundles characteristic for the IAA-free sample (Fig. 3, E and F), numerous fine cortical actin filaments were observed upon addition of 2 µM IAA (Fig. 3G) and even the transvacuolar strands were much finer than in the untreated control (Fig. 3H). This auxin effect was specific for IAA when 2 µM 2,4-D was added (in addition to the 0.9 µM corresponding to 0.2 mg/L of 2,4-D that was present in all samples); this had no effect on the arrangement of actin filaments (Fig. 3, I and J). How did these hormone treatments affect the pattern of cell division in the YFP-mT line? After addition of IAA, the synchrony of cell division, manifest as the characteristic pattern with elevated frequencies of even-numbered cell files, was restored in the YFP-mT cell line (Fig. 4D). In contrast, additional 2,4-D just shifted the frequency distribution toward higher cell numbers without restoring synchrony; the residual difference in the frequencies of even and uneven cell numbers was even lower than in the untreated control line (compare Fig. 4, G to A). When we tested the response of nontransformed control cells to IAA, we did not see any significant change of synchrony. The only effect consists of a slight shift of the distribution to higher cell numbers (compare Fig. 4, E to F). A treatment with 2 µM NAA, in contrast, was able to rescue the synchrony of cell division partially (Fig. 5C). However, NAA was clearly less effective than IAA. Summarizing these results, we observed that actin was constitutively bundled in a BY-2 line overexpressing YFP-mT. This bundling of actin interferes with the synchrony of cell division in such a way that the division pattern is affected. Addition of polarly transported auxins, but not an increase of auxin per se, could restore both a normal organization of actin and the synchrony of cell division.
Cell divisions were also synchronized in BY-2 cells. We observed a clear pattern of cell division consisting of elevated frequencies of even-numbered cell files (Fig. 1B). We further observed that a mild inhibition of polar auxin transport, which only slightly affects the rate of cell division (Fig. 1, F1 and F2) and leaves cell elongation unaffected (Fig. 1G1), equalizes the prevalence of files with even cell numbers (Fig. 1C). This effect is induced by not only NPA, but also by other phytotropins (such as TIBA; Fig. 5A ). The actual signal seems to be the intracellular accumulation of IAA produced by these phytotropins. We conclude this from the synergistic effect of low concentrations of IAA with low concentrations of NPA (Fig. 5B). We conclude that, in BY-2 as well, polar intrafile auxin transport and not auxin per se is responsible for the patterning of cell division.
These experiments confirmed that BY-2 is a suitable system to study auxin-dependent patterning of cell division. In the next step, we asked for the role of actin in the generation of this pattern. Our previous work has shown that the auxin response to actin involves changes in the bundling of actin filaments, with bundled actin being characteristic for a situation where auxin was depleted (Waller et al., 2002
Although the expression of fluorescent proteins fused to actin-binding domains has been used as a convenient tool to study the actin cytoskeleton in living cells, the dynamics and organization of F-actin may change due to the expression of the fusion protein. These changes may cause problems with transport or signaling processes affecting cell division and cell growth. As published by Ketelaar et al. (2004)
For this purpose, we used a transgenic BY-2 cell line overexpressing YFP-mT under control of the 35S promoter. To eliminate transformants with low expression activity, we applied a stringent selection regime. This resulted in a generally high level of expression leading to a very strong bundling of actin filaments (Fig. 3, E and F). This bundling was also shown by Kost et al. (1998) We were now able to show that the bundling of actin interferes with the auxin-dependent synchrony of cell division. As a consequence of the impaired coordination of the cell cycle, the difference in the incidence of files with even and uneven cell numbers was strongly reduced already in untreated YFP-mT cells (Fig. 4A), an effect that could even be enhanced by treatment with NPA, an inhibitor of polar auxin flux. Already low concentrations of NPA produced alterations in the frequency distribution that were observed in the nontransformed cell line only for higher concentrations of this inhibitor. For instance, already for 12 µM NPA, files with more than two cells had become very rare. In the nontransformed cell line, a higher concentration (30 µM NPA) was required to cause a similar effect (compare Fig. 4C to 1E). In other words, the NPA sensitivity was increased in the YFP-mT line. This was also evident when overall division activity was plotted over the concentration of NPA (Fig. 1, F1 and F2). Given the impact of actin filaments in cell division, the overexpression of YFP-mT might impair cell division as such. This might explain the slightly delayed growth of the YFP-mT line (Fig. 1A). However, NPA and YFP-mT have a multiplicative effect on the interference of the coupling signal, indicating that both factors target to the same signaling cascade. Thus, most certainly, the increased sensitivity to NPA in the YFP-mT line implies that the link between actin organization and synchrony of cell division is based on changes of the directional transport of auxin.
If this reasoning is correct, and the constitutively bundled actin as well as the impaired synchrony of cell division depends on polar auxin transport, this synchrony should be restored when the massive actin bundles in the YFP-mT line are replaced by a finer meshwork of detached microfilament strands. We have tested this prediction experimentally by supplementing the medium either with polarly transported auxins (IAA and NAA) or 2,4-D that is not excreted by the efflux carrier responsible for polar auxin flux (Delbarre et al., 1996 We observed that the synchrony of cell division characterized by elevated frequencies of even-numbered cell files was restored in the YFP-mT line after addition of IAA (Fig. 4D) and, to a lesser extent, of NAA (Fig. 5C). In contrast, additional 2,4-D had no effect on the affected synchrony of cell division in the YFP-mT line.
Several studies have linked the polarity of auxin transport to actin-dependent vesicle flow (for review, see Friml, 2003
The experiments by Geldner et al. (2001)
Future work will focus on two aspects of patterned cell division in BY-2 cells: How is this pattern perpetuated over time, when the number of cells in a file increases progressively? To follow the pattern over time, we will use markers of cell polarity such as PIN1 in conjunction with visualization of actin. When the arrangement of actin filaments is important for pattern formation, then the polarity of actin filaments would decide over patterning via the transport of components necessary for auxin signaling. Although it is not possible to measure auxin efflux in a cell-culture system directly, it might be possible to detect differences in the accumulation of intracellular, radioactively labeled auxin (Petrá
Tobacco Cell Cultures
The tobacco (Nicotiana tabacum L. cv BY-2) cell line (Nagata et al., 1992
The p35S-YFP-mT construct (Brandizzi et al., 2002
For biolistic transformation, gold particles (1.5–3.0 µm; Sigma-Aldrich) were coated with the YFP-mT vector construct according to a modified manual of BIO-RAD (PDS-1000/He Particle Delivery System manual). An amount of 1 µg DNA was used for transfection. DNA-coated gold particles were placed on macrocarriers (BIO-RAD). A cell suspension of 3-d-old BY-2 cells was filtrated onto filter paper. Filtrated BY-2 cells were placed in a particle gun that was constructed according to Finer et al. (1992)
NPA was synthesized by Dr. Wolfgang Michalke (Albert-Ludwigs-Universität Freiburg, Institut für Biologie III, Freiburg, Germany) according to Thompson et al. (1973)
Actin filaments were visualized by the method of Kakimoto and Shibaoka (1987) For the colocalization experiment of YFP-mT and rhodamine-phalloidin in BY-2 cells overexpressing YFP-mT, the same protocol was used.
From each sample, 0.5-mL aliquots of cells were collected 4 d after inoculation and immediately viewed under an AxioImager Z.1 microscope (Zeiss). Differential interference contrast images were obtained by a digital imaging system (AxioVision; Zeiss) and frequency distributions over the number of cells per individual file were constructed. Cell length and width were also determined from the central section of the cells using the length function of the AxioVision software. Each data point represents 3,000 cell files or cells from three independent experimental series. The results were tested for significance by a t test at the 95% confidence level.
Cell viability was analyzed by the Trypan Blue dye exclusion test (Phillips, 1973 For the mitotic indices, 0.5-mL aliquots of cell suspension were fixed in Carnoy fixative (3:1 [v/v] 96% [v/v] ethanol:glacial acetic acid) plus 0.25% Triton X-100 and stained with 2'-(4-hydroxyphenyl)-5-(4-methyl-1-piperazinyl)-2,5'-bi(1H-benzimidazole)-trihydrochloride (Hoechst 33258, Sigma-Aldrich), which was prepared as a 0.5-mg/mL filter-sterilized stock solution in distilled water and used at a final concentration of 1 µg/mL. Cells were recorded under an AxioImager Z.1 microscope (Zeiss) using the filter set 49 4',6-diamino-phenylindole (excitation at 365 nm, beamsplitter at 395 nm, and emission at 445 nm). The mitotic indices were calculated as the number of cells in mitosis divided by the total number of cells counted. For each time point, 1,000 cells were scored.
For morphological studies, cells were examined under an AxioImager Z.1 microscope (Zeiss) equipped with an ApoTome microscope slider for optical sectioning and a cooled digital CCD camera (AxioCam MRm). TRITC and YFP fluorescence were observed through the filter sets 43 HE (excitation at 550 nm, beamsplitter at 570 nm, and emission at 605 nm) and 46 HE (excitation at 500 nm, beamsplitter at 515 nm, and emission at 535 nm), respectively (Zeiss). Images were processed and analyzed using the AxioVision (Rel. 4.5) software as described above. For analysis of division pattern, cells were observed under the same microscope with a 20x objective and differential interference contrast illumination. Images were processed for publication by the Photoshop software (Adobe Systems). BY-2 cells were examined under an AxioImager Z.1 microscope (Zeiss) equipped with an ApoTome microscope slider for optical sectioning and a cooled digital CCD camera (AxioCam MRm). TRITC and RFP fluorescence were observed through the filter set 43 HE (excitation at 550 nm, beamsplitter at 570 nm, and emission at 605 nm). YFP and GFP fluorescence were recorded through the filter sets 46 HE (excitation at 500 nm, beamsplitter at 515 nm, and emission at 535 nm) and 38 HE (Zeiss; excitation at 470 nm, beamsplitter at 495 nm, and emission at 525 nm), respectively, using either a 63x plan apochromat oil-immersion objective or a 40x objective. Stacks of optical sections were acquired at different step sizes between 0.5 and 0.8 µm. Images were processed and analyzed using the AxioVision software (Rel. 4.5; Zeiss) as described above. For analysis of division pattern, cells were observed under the same microscope with a 20x objective and differential interference contrast illumination. For publication, images were processed with respect to contrast and brightness using the Photoshop software (Adobe Systems).
The authors thank Dr. Federica Brandizzi (Oxford Brooks University, UK) for the p35S-YFP-mT construct and Sabine Purper (Universität Karlsruhe, Germany) for excellent technical support. NPA was kindly provided by Dr. Wolfgang Michalke (Albert-Ludwigs-Universität Freiburg, Germany). Received December 3, 2006; accepted February 21, 2007; published March 2, 2007.
1 This work was supported by the Landesgraduierten-Programm of the State of Baden-Württemberg (fellowship to J.M.), and by the Landesschwerpunkt-Programm of the State of Baden-Württemberg (LuNaCell; to P.N.).  The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Jan Maisch (jan.maisch{at}botanik1.uni-karlsruhe.de). www.plantphysiol.org/cgi/doi/10.1104/pp.106.094052 * Corresponding author; e-mail jan.maisch{at}botanik1.uni-karlsruhe.de; fax 49–721–608–4193.
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ek et al., 2006
amaj, F Balu
imalová E, Ruthardt N, Petrá
erná A, Schwarzerová K, El
kner M, Morris DA, Za
niewska J, Tadele Z, Kube
