JXB Advance Access published online on January 22, 2007
Journal of Experimental Botany, doi:10.1093/jxb/erl274
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© 2007 The Author(s).
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/2.0/uk/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.This paper is available online free of all access charges (see http://jxb.oxfordjournals.org/open_access.html for further details)
RESEARCH PAPER |
Auxin response, but not its polar transport, plays a role in hydrotropism of Arabidopsis roots
Graduate School of Life Sciences, Tohoku University, Sendai, 980-8577, Japan
* To whom correspondence should be addressed. E-mail: miyazawa{at}ige.tohoku.ac.jp
Received 25 May 2006; Revised 16 November 2006 Accepted 17 November 2006
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Abstract |
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Plants are sessile in nature, and need to detect and respond to many environmental cues in order to regulate their growth and orientation. Indeed, plants sense numerous environmental cues and respond via appropriate tropisms, and it is widely accepted that auxin plays an important role in these responses. Recent analyses using Arabidopsis have emphasized the importance of polar auxin transport and differential auxin responses to gravitropism. Even so, the involvement of auxin in hydrotropism remains unclear. To clarify whether or not auxin is involved in the hydrotropic response, Arabidopsis seedlings were treated with inhibitors of auxin influx (3-chloro-4-hydroxyphenylacetic acid), efflux (1-naphthylphthalemic acid and 2,3,5-triiodobenzoic acid), and response (p-chlorophenoxyisobutylacetic acid), and their effects were examined on both hydrotropic and gravitropic responses. In agreement with previous reports, gravitropism was inhibited by all the chemicals tested. By contrast, only an inhibitor of the auxin response (p-chlorophenoxyisobutylacetic acid) reduced hydrotropism, whereas inhibitors for influx or efflux of auxin had no effect. These results suggest that auxin response, apart from its polar transport, plays a definite role in hydrotropic response, and will evoke a new concept for the auxin-mediated regulation of tropisms.
Key words: Arabidopsis, auxin, p-chlorophenoxyisobutylacetic acid (PCIB), gravitropism, hydrotropism
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Introduction |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Terrestrial plants are sessile and must complete their life cycles at the location where they germinated. As a result, they have evolved a remarkable capacity for morphological plasticity that enables them to adapt to surrounding conditions. One of the most important mechanisms underlying this plasticity is tropism, growth directed towards or away from a stimulus. Tropisms allow plants to utilize limited resources or to avoid unfavourable growing conditions. To date, plants have been shown to recognize a number of environmental signals that lead to tropic responses, such as gravity, light, touch, and moisture gradients. The responses to these stimuli are referred to as gravitropism, phototropism, thigmotropism, and hydrotropism, respectively. Despite the importance of these tropisms, only the gravitropic response has been studied extensively, since the effects of this tropism usually outweigh those of the other responses. Root hydrotropism was the subject of early classical investigations (reviewed in Takahashi, 1997). However, investigators paid little attention to this phenomenon for much of the last century, due to the difficulty of separating hydrotropism from gravitropism; it was not until 1985 that Jaffe et al. demonstrated a hydrotropic response, using an agravitropic pea mutant. Since that time, the roots of agravitropic mutant or of clinorotated seedlings have enabled hydrotropism to be separated from gravitropism in pea and cucumber (Jaffe et al., 1985; Takahashi and Suge, 1991; Takahashi et al., 1996; Mizuno et al., 2002). The results gained from these experimental systems suggest that gravitropism interferes with hydrotropism in these species. Moreover, it has been found that the water potential gradient is sensed in the root cap cells, where gravistimulus is also sensed (Takano et al., 1995). Recently, an experimental system was established using a model plant species, Arabidopsis thaliana. It was found that hydrotropism interacts with gravitropism by degrading starch in response to the moisture gradient (Takahashi et al., 2002, 2003). However, neither common nor distinct mechanisms that contribute to this interaction have been identified to date.
Auxin, the first phytohormone to be defined, plays a central role in many aspects of plant morphogenesis. Extensive studies led to several discoveries concerning the mechanisms of auxin transport, distribution, and reception, as well as its signal transduction (reviewed in Weijers and Jürgens, 2004; Kramer and Bennett, 2006). The Cholodny–Went hypothesis holds that the detection of environmental stimuli leads to lateral auxin redistribution; recent molecular genetic analyses have demonstrated that, for the most part, the hypothesis holds for the gravitropic response. A number of molecules that are crucial for auxin redistribution and auxin response have been identified (reviewed in Paciorek and Friml, 2006). In addition, it has been found that hydrotropism involves asymmetric expression of an auxin-inducible gene in hydrotropically bending cucumber seedlings, suggesting that auxin redistribution is involved in this response (Mizuno et al., 2002). On the other hand, it has also been found that some Arabidopsis mutants that have defects in auxin polar transport show a normal hydrotropic response, a result that conflicts with the model established from previous gravitropism research (Takahashi et al., 2002). Since auxin distribution is crucial for tropic growth, the questions of whether or not auxin also plays an important role in the hydrotropic response, and how its redistribution under that response is differentiated from that under the gravitropic response, remain to be addressed.
In order to answer the above questions, wild-type Arabidopsis seedlings were treated with inhibitors that nullify auxin influx, efflux, or response, and their responses to either gravitropic or hydrotropic stimuli compared with those of untreated seedlings. The use of inhibitors has two advantages over the use of mutants: (i) each inhibitor can be treated as a pulse, thus negating the possibility of disorganized development, a phenomenon often observed in auxin mutants; (ii) treatment with inhibitors can be used in a time-specific manner to nullify processes that are of interest. Recent research using mutants has indicated that the products of PIN-FORMED 1 and its homologues (PINs) have compensatory properties: loss of expression of a specific PIN is compensated for by auxin-dependent ectopic expression of its homologues (Vieten et al., 2005). Using inhibitors, it is possible to negate this functional redundancy. In the present study, it is shown that treatment of Arabidopsis roots with an inhibitor of the auxin response reduces the development of hydrotropic curvature, whereas application of polar auxin transport inhibitors does not. As inhibitors of both auxin polar transport and auxin response are inhibitory to the development of gravitropic curvature, these results suggest that hydrotropism involves a novel mechanism of auxin-dependent differential growth that is distinguishable from that of gravitropism.
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Materials and methods |
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Plant growth conditions
Seeds of Arabidopsis thaliana (ecotype Columbia) were sterilized with a solution containing 5% (v/v) sodium hypochlorite and 0.05% (v/v) Tween 20 for 5 min, washed with distilled water, and germinated on 0.2% Gellan Gum (Sigma, St Louis, MO, USA) plates of half-strength Murashige and Skoog medium (Sigma), as described in Takahashi et al. (2003). Upon germination, plates were set in a vertical position so that the seedlings grew straight along the surface of the medium. The seedlings were then grown in an incubator at 23 °C under continuous light. Seedlings with straight roots, 1.0–1.5 cm in length, were used for the experiments.
Treatment with inhibitors
1-Naphthylphthalemic acid (NPA; Tokyo Kasei Kogyo Co., Tokyo, Japan) and 2,3,5-triiodobenzoic acid (TIBA; Sigma) were used as inhibitors of auxin efflux carriers, and 3-chloro-4-hydroxyphenylacetic acid (CHPAA; Tokyo Kasei Kogyo Co.) was used as an inhibitor of auxin influx carriers. In addition, p-chlorophenoxyisobutylacetic acid (PCIB; Tokyo Kasei Kogyo Co.) was used to inhibit auxin responses. All inhibitors were prepared at 1000x concentration in dimethyl sulphoxide (DMSO). For control cultures, an equivalent volume of DMSO was added to the medium. The seedlings were pretreated on 1% agar medium containing inhibitor for 90 min prior to the assays (Fig. 1A).
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Hydrotropism assay using moisture gradient
Roots were stimulated hydrotropically according to the method of Takahashi et al. (2002), with slight modifications. In brief, a moisture gradient for the induction of hydrotropism was established between 1% (w/v) agar (Wako Chemical Co., Osaka, Japan) plates and a saturated solution of K2CO3, in a closed acrylic chamber. The seedlings were placed vertically on the inhibitor-containing 1% agar plates, with the root tip (approximately 0.2 mm in length) suspended freely from the edge of the agar (Fig. 1A). The chambers were then placed in the dark at 24 °C. All seedlings were photographed under a stereomicroscope (SZH-ILLB; Olympus, Tokyo, Japan). Measurements of root growth and hydrotropic curvature were performed using the NIH Image software. Statistical differences for these and all following assays were determined using Student's two-tailed t test at P <0.05.
Agar medium-based hydrotropism assay
Agar medium-based hydrotropism assays were performed according to Takahashi et al. (2002) with slight modification. Two triangular plates, one containing 1% (w/v) plain agar and the other containing sorbitol, were placed side-by-side in a plastic plate (Fig. 6A). Arabidopisis seedlings were aligned on the agar plate with their root tips 1 cm away from the junction of two agar plates. Then the plate was covered with a cap and sealed with surgical tape. The apparatus was incubated at 23 °C in the dark. All plates were photographed using an image scanner at a resolution of 1200 dpi (A850; Seiko Epson Corp., Nagano, Japan). For control experiments, DMSO was added to make an equivalent concentration. Measurements of root growth and hydrotropic curvature were performed using the NIH Image software.
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Gravitropism assay
Seedlings were placed vertically on inhibitor-containing 1% (w/v) agar plates, which were then re-orientated 90° and placed in the dark at 24 °C. All seedlings were photographed under a stereomicroscope. Root growth and gravitropic curvature were monitored as described above.
Microscopic observations of starch granules
Seedlings were fixed in a solution containing 45% (v/v) ethanol, 5% (v/v) formaldehyde, and 5% (v/v) acetic acid at 4 °C for 48 h. The fixed seedlings were then rehydrated using an ethanol:water series (50%:50%, 25%:75%, and 0%:100%, for 15 min each). Starch granules were stained with Lugol's solution (Merck, Darmstadt, Germany) as described in Miyazawa et al. (2002). Following staining, seedlings were observed under a microscope (IX-71; Olympus) and photographed using a model DP70 camera (Olympus). To measure stained areas, photographs were analysed using the NIH Image software.
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Results |
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Figure 1A depicts the experimental system used in the study. When the root tips were suspended vertically from the agar plate in the presence of a moisture gradient, the roots bent towards the agar and deviated 30–50° from vertical within 4 h of exposure to the moisture gradient (Fig. 1B). After 8 h of hydrostimulation, the hydrotropic curvature was approximately 90°. In the saturated-air chamber, roots placed in a vertical position on the agar plate displayed gravitropism, with curvatures ranging from 0° to 10°, but never to a higher degree over the course of the 8 h experiment. There was a significant difference in curvature between the hydrostimulated and control roots at 4 h and 8 h after the start of the experiment. Regardless of the presence or absence of the humidity gradient, root growth did not differ significantly between groups (Fig. 1B). Previous results, in which the asymmetric expression pattern of auxin-inducible genes was induced in hydrotropically responding cucumber roots, indicated that auxin response contributes to this tropism (Mizuno et al., 2002). To gain further insight into the mechanisms of auxin involvement in the hydrotropic response, several inhibitors that nullify auxin influx, efflux, and response were used and their effects on hydrotropism examined. Inhibitors were chosen that have been characterized in previous tropism studies: CHPAA as an inhibitor of auxin influx; NPA or TIBA as inhibitors of auxin efflux; and PCIB as an inhibitor of auxin responses (Muday, 2001; Parry et al., 2001; Oono et al., 2003). To confirm that the drugs were administered effectively, their effects on gravitropism were also examined.
Initially, the effect of CHPAA, an inhibitor of the auxin influx carrier, was investigated on hydrotropic and gravitropic growth (Fig. 2). CHPAA treatment significantly decreased the development of gravitropic curvature in a dose-dependent manner, a result that confirmed the findings of Parry et al. (2001), showing that the inhibitor treatment is effective. Unexpectedly, CHPAA treatment did not interfere with the development of hydrotropic curvature, even at concentrations at which gravitropism was suppressed. Moreover, when seedlings were treated with CHPAA at a concentration of 10–5 M, a slight enhancement of the hydrotropic response was observed 4 h after the start of the experiment. Overall, root growth rates were unaltered by CHPAA treatment, regardless of concentration. These results suggest that the auxin influx carrier plays no role in the root hydrotropic response in Arabidopsis.
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Next, seedlings were treated with inhibitors that nullify auxin efflux, using various concentrations of two inhibitors of different classes, i.e. NPA and TIBA. When seedlings were treated with >10–6 M NPA, development of gravitropic curvature was reduced in a dose-dependent manner. NPA (10–5 M) severely impaired both gravitropic response and root growth rate (Fig. 3). By contrast, when NPA-treated seedlings were hydrostimulated, no effect on hydrotropic curvature was observed, even at concentrations at which root growth was inhibited (Fig. 3A). This observation was further supported by the TIBA treatment results (Fig. 4). TIBA treatment severely reduced the development of gravitropic root bending in a dose-dependent manner, an effect accompanied by a slight decrease in root growth rate. Again, treatment of TIBA had no effect on hydrotropism, although there was a slight decrease in root growth rate at 10–5 M. These results strongly suggest that auxin efflux carriers are not necessary for the hydrotropic response.
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Also the effects of PCIB, an inhibitor of auxin response, were examined on both hydrotropism and gravitropism. Although a significant reduction in gravitropic curvature was observed at 10–6 M, PCIB, no significant decrease in root growth rate was observed at this concentration (Fig. 5). The effect became more marked at 10–5 M, at which concentration a reduction in root growth rate was also observed. PCIB treatment also inhibited the hydrotropic response at 10–5 M, but not at 10–6 M, the concentration at which the gravitropic response was significantly reduced (Fig. 5). Thus, the hydrotropic response appears to be less sensitive than the gravitropic response to the effects of auxin. Although a reduction in root growth rate (28% less than the controls) was observed at 4 h, it is believed that this had a negligible effect on the development of the curvature (54% less than the controls; Fig. 5).
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Because the above-mentioned experimental system needs Arabidopsis root tips to be detached from the agar medium, it may be likely that some of the inhibitors were not effective. From this reason, the present observations were further confirmed by using an agar medium-based hydrotropism assay (Takahashi et al., 2002; Fig. 6). Hydrotropic response was observed only when Arabidopsis seedlings were exposed to an osmotic gradient made between plain agar and sorbitol-containing agar (Fig. 6A, B). The development of the curvature was almost saturated at 24 h after starting the experiment. When CHPAA was added to the medium, no significant decrease or increase in the development of hydrotropic curvature was observed (Fig. 6C). Similarly, neither NPA nor TIBA treatment inhibited the development of the hydrotropic curvature, but rather they tended to increase the development of the curvature. On the other hand, PCIB significantly inhibited the development of the hydrotropic curvature.
The hydrotropic curvature kinetics in the PCIB-treated seedlings were examined further (Fig. 7). When the seedlings were hydrostimulated, the effect of PCIB treatment on root curvature became obvious at 2 h, and the effect grew more evident over time. Conversely, when the root tips were suspended in fully saturated air, the PCIB-treated seedlings did not deviate from the vertical and showed a growth pattern similar to that of the control seedlings. From these results, it was concluded that auxin response, but not auxin polar transport, plays an indispensable role in root hydrotropism of Arabidopsis.
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Previously, it had been demonstrated that development of the hydrotropic response was accompanied by a simultaneous reduction in the starch content of columella cells, reducing the gravitropic response and enabling the roots to exhibit hydrotropism in the presence of gravity (Takahashi et al., 2003). To test the hypothesis that the reduction in hydrotropic response observed in PCIB-treated seedlings involves reduced amyloplast degradation, columella starch content was monitored in treated and control seedlings, but no significant differences were found (Fig. 8). This result suggests that the reduced development of hydrotropic curvature induced by PCIB treatment was not a result of enhanced gravitropism caused by the inhibition of starch degradation, but of inhibition of an asymmetric auxin response.
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Discussion |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Auxin is a phytohormone required for many aspects of plant development, including cell division, apical dominance, and differential growth, and its involvement in differential growth is predicted by the Cholodny–Went hypothesis (Went and Thimann, 1937). Indeed, redistribution of auxin across gravistimulated organs has been shown to be crucial for gravitropism, the most well characterized of the tropic responses (reviewed in Muday, 2001). Recent molecular genetic analyses of Arabidopsis have identified the auxin-related molecules that function in the gravitropic response in roots (Friml et al., 2002; Liscum and Reed, 2002; Swarup et al., 2005; Abas et al., 2006). These molecules fall into three activity categories: auxin influx, auxin efflux, and auxin action. Previously, it had been shown that differential expression of an auxin-inducible gene occurred in clinorotated, hydrotropically responding cucumber seedlings, which led to the idea that auxin redistribution may also be involved in hydrotropism (Mizuno et al., 2002). Recently, a system for the induction and measurement of the hydrotropic response in Arabidopsis seedling roots was developed, and a hydrotropic response in the presence of gravity was observed (Takahashi et al., 2002). Moreover, a previous study of Arabidopsis agravitropic mutants (aux1-7, wav6-52, axr2-1, and axr1-3) showed no observable reduction in hydrotropic response, which rendered the importance of auxin in hydrotropism somewhat obscure (Takahashi et al., 2002). Since the genes responsible for auxin efflux and response exhibit functional redundancy (Liscum and Reed, 2002; Viten et al., 2005), it was decided to investigate the effects of chemicals with specific patterns of inhibition in order to determine not only whether or not auxin plays a role in hydrotropism, but also how auxin redistribution under the hydrotropic response is differentiated from that under gravitropism.
In the present study, it was demonstrated that inhibitors of auxin influx and efflux had no effect on hydrotropism, whereas they severely inhibited gravitropism (Figs 2–4
, 6C), a result that concurred with previous findings (reviewed in Blancaflor and Masson, 2003). These results also concurred with those of previous studies using agravitropic Arabidopsis mutants (Takahashi et al., 2002), and these findings, taken together, suggest that auxin carriers, which have been identified to date, play no role in hydrotropism.
Furthermore, it was demonstrated that treatment with PCIB, an auxin response inhibitor, resulted in a decrease in both hydrotropic and gravitropic curvatures. The results for gravitropism concur with a previous report (Oono et al., 2003) and confirm the validity of the inhibitor treatment. Owing to the structural similarities of the two molecules, it is believed that PCIB binds competitively to the auxin-binding site, thereby inhibiting the auxin response. Accordingly, the reduction of hydrotropism under PCIB treatment strongly suggests a role for auxin response in this process. However, it had been reported previously that the roots of the auxin-resistant mutants axr1-3 and axr2-1 did not display any decrease in hydrotropic response, a finding that would appear to contradict those of the current study (Takahashi et al., 2002). Although, the exact mechanism that causes this apparent discrepancy is not known, it is likely that auxin action in hydrotropic response is not entirely the same as that in gravitropism. AXR1 has been shown to encode part of a heteromeric RUB-activating enzyme that modifies the SCFTIR1 subunit required for degradation of Aux/IAA proteins, a family that negatively regulates auxin-mediated transcription (reviewed in Weijers and Jürgens, 2004). The hydrotropic response may comprise a set of auxin-regulated cascades unrelated to AXR1 function, whereas the gravitropic response may comprise an additional auxin-regulated cascade governed by AXR1. Indeed, the axr1-3 mutant displays a slower, but definite, response to gravity when compared with wild-type plants (Lincoln et al., 1990). The present data also support the suggestion that the effective concentration of PCIB differs between the hydrotropic and gravitropic responses, with the former being more resistant to PCIB than the latter (Fig. 5). Moreover, recent studies suggested that two stabilized Aux/IAA proteins confer different responses on the same cell, and auxin responses are further specified by optimized pairs of interacting Aux/IAA–ARF proteins (Knox et al., 2003; Weijers et al., 2005). It will be important, in the future, to use auxin mutants other than axr1-3 and axr2-1 for elucidating the auxin-related molecules that regulate hydrotropic response in Arabidopsis. Alternatively, Eapen et al. (2005) discussed that the changes in growth direction in these mutants might be the consequence of their random root growth caused by their agravitropism. Indeed, in the experimental system using moisture gradient as the hydrostimulus, seedling roots are suspended so as to move freely. However, the present result using an agar-based experimental system clearly demonstrated that among the inhibitor treatments that confer agravitropic responses, only the PCIB treatment caused ahydrotropic growth (Fig. 6C).
Recently, Eapen et al. (2003) isolated and characterized nhr1, a hydrotropic Arabidopsis mutant. The root tips of this mutant exhibit abnormal morphology, with an enhanced response to gravity that is likely to be the result of abnormally large amyloplasts in the columella cells. It has been suggested that for the hydrotropic response to overcome the gravitropic response, it is important that amyloplast degradation occurs following hydrostimulation (Takahashi et al., 2003). Therefore, one might assume that PCIB treatment would inhibit amyloplast degradation, thereby reducing the hydrotropic response. However, the present results indicate that in PCIB-treated seedlings, amyloplast degradation occurred to a similar extent to that observed in control seedlings, suggesting that this inhibitor specifically affected auxin-mediated differential growth.
At present, the mechanisms underlying the regulation and progression of the auxin-mediated hydrotropic response remain unclear. Nevertheless, it was found that not the auxin polar transport, but its response, plays a definite role in hydrotropism. Thus, the present results suggest the presence of a novel mechanism for auxin-mediated growth regulation.
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Acknowledgements |
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The authors thank Ms Yoko Kakimoto (Tohoku University) for her technical assistance. This work was supported by the Program for Promotion of Basic Research Activities for Innovative Biosciences (PROBRAIN) to YM, Grants-in-aid for Scientific research (B) (No. 16380166) from JSPS and for Scientific Research on Priority Areas (No. 170510003) from MEXT, and grants from the Takeda Science Foundation to HT. This study was also carried out as part of the ‘Ground-based Research Announcement for Space Utilization’ promoted by the Japan Space Forum.
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