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Plant Physiology 132:1085-1096 (2003) © 2003 American Society of Plant Biologists Ethylene Modulates Root-Wave Responses in Arabidopsis1,[w]Plant Cell Biology (C.S.B., G.O.W.), and Environmental Biology Groups (C.S.B., J.M.), The Institute of Advanced Studies, Research School of Biological Sciences, The Australian National University, G.P.O. Box 475, Canberra, Australian Capital Territory 2601, Australia
When stimulated to bend downward by being held at 45 degrees off vertical but unable to penetrate into agar-based media, Arabidopsis roots develop waving and looping growth patterns. Here, we demonstrate that ethylene modulates these responses. We determined that agar-containing plates sealed with low-porosity film generate abiotic ethylene concentrations of 0.1 to 0.3 µL L-1, whereas in plates wrapped with porous tape, ethylene remains at trace levels. We demonstrate that exogenous ethylene at concentrations as low as a few nanoliters per liter modulates root waving, root growth direction, and looping but through partly different mechanisms. Nutrients and Suc modify the effects of ethylene on root waving. Thus, ethylene had little effect on temporal wave frequency when nutrients were omitted but reduced it significantly on nutrient-supplemented agar. Suc masked the ethylene response. Ethylene consistently suppressed the normal tendency for roots of Landsberg erecta to skew to the right as they grow against hard-agar surfaces and also generated righthanded petiole twisting. Furthermore, ethylene suppressed root looping, a gravity-dependent growth response that was enhanced by high nutrient and Suc availability. Our work demonstrates that cell file twisting is not essential for root waving or skewing to occur. Differential flank growth accounted for both the extreme root waving on zero-nutrient plates and for root skewing. Root twisting was nutrient-dependent and was thus strongly associated with the looping response. The possible role of auxin transport in these responses and the involvement of circadian rhythms are discussed.
Plants, as sessile organisms, require flexible growth responses to adapt to stressful conditions, including stresses related to soil mechanical strength. To penetrate soils, roots must displace or deform soil aggregates. Even in the loosest soils, root tips experience combinations of mechanical forces, one of which is touch. Roots are very sensitive to touch, and thigmomorphogenic responses have been studied under a variety of experimental systems ranging from exogenous applications of transient forces to gravity-induced tests (e.g. Goss, 1977  ; Wilson et al., 1977; Okada and Shimura, 1990; Legué et al., 1997). One extensively studied morphological response is root waving. Since Okada and Shimura (1990) first described and attributed the wave-like growth in the Landsberg erecta (Ler) ecotype of Arabidopsis to a gravity-induced touch response, Simmons et al. (1995) and Mullen et al. (1998) hypothesized that gravity and/or circumnutation provided the stimuli. Although phenotypes are well described at the whole-root level, the underlying cellular mechanisms are not well understood. We recently discovered that the gaseous environment within a petri plate could override gravitational effects on root waving, although the causal agent(s) remained unidentified (Buer et al., 2000). Wrapping plates with a porous material that allows gas exchange between the atmosphere and the inside of the plate, as opposed to a low-porosity material that inhibits gas exchange, produced remarkably different root phenotypes. These phenotypes ranged from straight growth to waving or looping depending on nutrient conditions. Moreover, plants growing in sealed plates developed increased root hair densities, radial root expansion, decreased root elongation, reduced leaf expansion, and cotyledon epinasty, all phenomena associated with ethylene exposure (Baskin and Williamson, 1992; Kieber et al., 1993; Masucci and Schiefelbein, 1994; Tanimoto et al., 1995; Smalle and van der Straeten, 1997; Pitts et al., 1998). This led us to hypothesize that ethylene signaling was involved in controlling root waving and the morphological differences observed between seedlings grown in aerated and sealed plates. Ethylene gas regulates many growth processes and stress responses in plants (Mattoo and Suttle, 1991; Abeles et al., 1992). Many morphological changes in impeded roots mimic changes that occur during ethylene exposure (Masle, 2002). Ethylene is evolved during root mechanical impedance (e.g. maize [Zea mays]; Kays et al., 1974; Sarquis et al., 1991) and has been identified as one of the root signals causing reduced root and leaf elongation in impeded tomato (Lycopersicon esculentum) plants (Hussain et al., 1999, 2000). Ethylene interactions seem complex. Ethylene cross-talks with other growth regulators (abscisic acid [Beaudoin et al., 2000], auxin [Rahman et al., 2001], cytokinins [Cary et al., 1995], and gibberellins [Ghassemian et al., 2000; Rahman et al., 2000]) and is also involved in Suc signaling (Zhou et al., 1998; Gibson, 2000). We conducted experiments to test whether ethylene acts as a modulator of root waving and associated morphological responses in Arabidopsis. We held the gravity vector constant and manipulated exogenous ethylene concentrations around seedlings growing on the surface of tilted agar plates. We demonstrate that ethylene is a key factor in the control of morphogenetic responses in roots repetitively challenged by a gravity-induced mechanical stimulus. Furthermore, we show that ethylene effects on root waving, root looping, cell file twisting, and differential flank growth are modulated by Suc and nutrient ion concentrations in the agar. Whether these interactions entirely reflect a direct influence of Suc and nutrients on ethylene signaling or also indicate Suc and ionic effects on the physical properties of the medium, including its surface characteristics, remains to be established.
Agar-Containing Plates Evolve Significant Levels of Ethylene Gas chromatography was used to determine ethylene concentrations in the headspace of petri plates wrapped with Nescofilm, a paraffin-based film (hereafter sealed plates) or with surgical tape (hereafter aerated plates). Figure 1 shows these concentrations over a 7-d period with d 1 corresponding to the 2nd d after plate preparation and, for plates with seedlings, to the day when most seeds germinated. Aerated plates containing plants had nearly undetectable levels of ethylene. In sealed plates, however, ethylene concentrations varied between 0.1 and 0.3 µL L-1. Remarkably, these concentrations were not significantly affected by the presence or absence of seedlings in the plate, demonstrating that the measured ethylene was mostly of abiotic origin. Furthermore, Figure 1 indicates that larger amounts of ethylene were evolved in plates in which the agar was not supplemented with nutrients (zero nutrient plates). The addition of KMnO4 crystals lowered the ethylene concentrations within sealed plates to 0.03 µL L-1 or less.
To test the influence of exogenous ethylene on root morphogenesis and waving phenotypes, we directly manipulated ethylene concentrations within the plate headspace. Our previous study showed ionic effects on root waving and looping, suggesting ethylene: nutrient interactions (Buer et al., 2000
Our earlier observations indicated there is a correlation between root elongation rate, spatial density, and amplitude of waving (Buer et al., 2000 Manipulating exogenous ethylene concentrations caused a wide range of root-waving and morphogenetic phenotypes, shown pictorially in Figure 2 and quantitatively in Figure 3. Ethylene increased root hair density and root diameter (45% and 27%, respectively, under zero nutrient conditions [Fig. 2, A–D]). It stimulated cotyledon epinasty (Fig. 2, E, F, K, and L) and reduced seedling growth (Figs. 2, E–H and I–O, and 3A). Ethylene increased the tightness of root bending regardless of nutrient supplementation (Fig. 2) and, under zero nutrient conditions, it dramatically increased the spatial frequency of root waving (Fig. 3B). These data unambiguously demonstrate a role for ethylene in the modulation of root waving on a spatial scale.
The data in Figure 3 indicated an inverse correlation between the effects of ethylene on root elongation rate and on the spatial frequency of waving (compare trends in Fig. 3, A and B). Figure 4 depicts the overall quantitative relationship between the two parameters, across the range of nutrients, Suc, and ethylene concentrations analyzed in this study. The individual values recorded for all treatments fell along a common curve, with the number of waves per unit root length decaying exponentially as roots elongated faster, either because nutrients were added to the medium, or because ethylene concentrations around the seedlings were lowered. Therefore, to determine whether ethylene had direct effects on the signaling of waving in roots, independent of growth effects, we examined the rhythm of waving (Fig. 3C). Waving frequency was calculated on a temporal basis (number of waves per unit of time). On zero nutrient plates, waves were produced at a frequency of about one wave per day (Fig. 3C, black bar). Wave production was little affected by variations in ethylene concentrations, except at the highest concentration of 1 µL L-1, which generated an approximately 25% lower waving frequency (Fig. 3C, black bar, treatment 5). In contrast, on Okada and Shimura-supplemented plates, exposure to 1 µL L-1 ethylene reduced the wave frequency almost 3-fold in comparison with wave frequencies detected at the lowest ethylene levels (Fig. 3C, hatched bar). On Murashige and Skoog-supplemented agar, the wave frequency was approximately halved in sealed plates (0.1–0.3 µL L-1 ethylene) compared with aerated plates (trace ethylene levels; data not shown). This demonstrates that ethylene can directly modulate the rhythm of root waving but that the extent of modulation is nutrient dependent.
Ethylene reduced the characteristic righthanded skewing of roots of the Ler ecotype (e.g. Fig. 2, N and O). This was observed on both nutrient-deprived and -supplemented plates (Fig. 3D), with a greater than 10° lefthanded shift (i.e. toward the vertical) in the root axis angle as ethylene concentrations increased from 1 nL L-1 to 1 µL L-1. This suppression of root skewing was correlated with the inhibition of root elongation rate by ethylene (Fig. 3, compare A and D).
There is compelling evidence for a direct role for nutrient ions, especially nitrogen (for review, see Forde, 2001
Ethylene clearly influenced the effects of Suc on root skewing (Fig. 5, C, F, and I). In sealed plates (0.1–0.3 µL L-1 ethylene), Suc addition did not alter root skewing. In the ethylene-free (aerated) plates, however, Suc caused roots to skew further to the right when nutrients were supplied (Fig. 5, C and F) and caused an opposite shift i.e. toward the vertical on zero-nutrient plates. Interestingly, these shifts in root axis angle with increasing Suc concentration were not always correlated with Suc effects on root elongation rate (compare Fig. 5, B and C), showing that the two parameters are not intrinsically linked.
The frequency of looping was plotted against ethylene concentrations for all conditions under which it was recorded (Fig. 6). Manipulating Suc and nutrient concentrations in the agar within both aerated and sealed plates revealed their role and interactions with ethylene in the signaling of root looping. Suc promoted root looping, but ethylene overrode these effects. Looping was rarely observed on zero-nutrient plates (Fig. 6,
Previous studies have consistently reported cell file twisting in roots that either wave or skew across tilted agar plates. To determine whether root twisting is an essential component of root-waving, -skewing, and -looping phenotypes, cryo-stage scanning electron micrographs were taken of roots grown under the various conditions described in this study. Under zero-nutrient conditions, no cell file rotation could be detected in wavy roots irrespective of plate aeration and Suc concentration (Fig. 7, A–D). Roots growing on nutrient-supplemented agar often showed alternating lefthanded and righthanded twisting of epidermal cell files according to the direction of root elongation, (Fig. 7, E and G). This was not always the case, however, as exemplified in Figure 7F, even in roots that traversed across the agar surface while continuing to wave (Fig. 8). All looping roots were characterized by pronounced cell file twisting (Fig. 7H); that twisting was always lefthanded in clockwise loops. Interestingly, in sealed plates or plates in which high concentrations of ethylene were injected (1 µL L-1), a slight righthanded cell file twisting was visible on petioles (Fig. 7I). No such response could be detected in aerated plates (Fig. 7J) nor in any of the plates from which nutrients had been omitted (not shown).
The above results demonstrated the involvement of differential flank growth in root waving, especially in roots in which cell file rotation could not be detected. To explore the possibility that this could be caused by changes in auxin distribution, we examined the influence of the polar auxin transport inhibitor 1-N-naphthylphthalamic acid (NPA; Lomax et al., 1995
Exogenous Ethylene Modulates Root Tropisms and Can Override Effects of Gravity-Induced Mechanical Stimulus
Roots growing in soil face complex conditions. They are continuously exposed to gravity, encounter mechanical forces that constrain their growth, and experience unpredictable changes in nutrient, carbon, and water availability. The aim of this work was to uncouple and create controlled variations of these parameters to assess their role in root morphogenesis. Our specific goal was to determine how ethylene affects the movement of Arabidopsis roots, which include waving or looping and, in the Ler ecotype, a tendency to skew to the right as they elongate along a hard agar surface. The possibility that ethylene was involved arose from our recent observations (Buer et al., 2000
Our experiments demonstrate that the buildup of ethylene in sealed plates can account for the differences in root phenotypes we reported earlier (Buer et al., 2000
By injecting ethylene into the headspace of aerated plates, or by oxidizing the ethylene evolved in sealed plates with KMnO4, we obtained reversion of root phenotypes, between straight growth and waving or looping or between vertical growth and skewing, despite no change in gravity or mechanical stimulus to the growing root tip. These effects occurred across a range of ethylene concentrations, from a few nanoliters per liter to about 100 nL L-1. Previous observations that ethylene causes roots to coil (Ipomoea pentaphylla [Vyas et al., 1973
Root waving, looping, and skewing all respond to ethylene but in different ways. Ethylene corrects for the ecotype-specific righthanded skewing of roots across the agar surface and does this consistently across a range of nutrient and Suc conditions. In contrast, the inhibitory effect of ethylene on root looping requires both Suc and nutrients. Root-waving responses to ethylene are more complex. Ethylene generally promotes dense waving (Figs. 2 and 3) but partly through a reduction on root elongation rates. When these effects are accounted for, and temporal waving frequencies are examined, complex interactions are revealed between ethylene, Suc concentration, nutrient availability, and composition (Figs. 3 and 5). Ethylene slows down waving in the presence of nutrients while having little effect in their absence (Figs. 3 and 5). Suc addition reduced this response or completely overrode it (Murashige and Skoog medium and Okada and Shimura medium, respectively). These observations demonstrate for the first time an antagonism between ethylene and Suc in the control of the root waving and looping phenotypes and add to the increasing evidence for cross-talk between the ethylene- and Suc-signaling cascades. Furthermore, they indicate that this ethylene: Suc antagonism is nutrient dependent. Recent studies of sugar-insensitive mutants indicate that a sugar: ethylene antagonism also operates in cotyledons and shoots for the control of many developmental transitions (Zhou et al., 1998
The observed interactions between ethylene and nutrient ions in modulating root waving and looping constitute a novel finding. Whether nutrients act directly on the ethylene-signaling cascade and/or indirectly by changing the chemical and mechanical properties of the agar and the amounts of ethylene it releases (Fig. 1) needs to be established. Further experiments are also required to ascertain which ions are involved. The observed differences between roots grown on Murashige and Skoog or Okada and Shimura media, however, suggest nitrogen ions may be the key element. The two media differ in composition, notably in their nitrogen contents. The Okada and Shimura formulation is low in nitrate (4.5 mM) and contains no ammonium ions (Somerville and Ogren, 1982
It was recently proposed that root-waving and -skewing patterns in Arabidopsis roots are both the consequence of the intrinsic root righthandedness and pronounced chirality seen in certain ecotypes (Migliaccio and Piconese, 2001
Overall, these results lead to the conclusion that root waving and skewing may result from two categories of processes driven by partly separate mechanisms: twisting and differential flank growth. Differential flank growth was clearly sufficient to drive waving and skewing in zero nutrient plates and on Okada and Shimura medium free of Suc, whereas some amount of root twisting may assist bending under nutrient- and Suc-supplemented conditions. Ethylene has been shown to influence cell wall extensibility (Smalle et al., 1997 Under conditions that enhanced skewing and looping responses (nutrient and Suc supplements), there was a clear bias for lefthanded helical twisting of roots. In those conditions, ethylene diminished, abolished, or even reversed looping and skewing and also generated righthanded twisting of petioles. One possible interpretation of these observations is that ethylene's modulation of looping and skewing is in fact a stimulation of righthanded twisting rather than a moderation of the nutrient and Suc-stimulated lefthanded twisting. If so, however, one would expect to see righthanded twisting in roots grown on zero-nutrient plates, which was not the case. One cannot therefore here separate between a direct ethylene signaling on root twisting or an indirect signaling, via effects on nutrient and Suc signaling pathways.
Our data suggest an endogenous circadian rhythm is involved in root waving, especially in the differential flank growth component. On zero-nutrient plates, where the most pronounced waving occurred in the absence of cell file twisting, the periodicity of waving was remarkably stable over a wide range of ethylene concentrations (Fig. 3C) and root elongation rates (Fig. 3A). A new wave was formed approximately every 24 h in the absence of photoperiodic clues, as seedlings were grown under continuous light. The expression of this free-running rhythm appears to depend on complex nutrient:Suc interactions (Fig. 5) with Suc addition causing a dramatic decrease in the wave period in the presence of nutrients, but a marked increase in period when nutrient supplements were omitted. Such interactions are consistent with increasing evidence for the involvement of circadian clocks in the control of ethylene, nitrogen, and sugar signaling (McClung, 2001
Plant Culture
Arabidopsis (ecotype Ler) seeds were surface-sterilized and sown on petri plates ( The plates were wrapped with a low-porosity paraffin-based film similar to Parafilm (Nescofilm, Azwell Inc., Osaka; labeled "sealed plates") or with gas permeable surgical tape (Micropore, 3M Health Care, St. Paul; labeled "aerated"). In all experiments, plates were placed in a growth chamber (Conviron, Controlled Environments, Pembina, ND) fitted with cool-white fluorescent tubes and incandescent bulbs providing 100 µmol quanta m-2 s-1 continuous light and maintained at 21°C temperature and 80% relative humidity. The plates were placed in racks where they were maintained at a 45° angle between the root growth axis and the gravity vector.
The growth racks were either open and in direct contact with the chamber atmosphere or were enclosed in sealed Perspex boxes (i.d. 115 x 125 x 275 mm, volume
Ethylene concentrations in the plate headspace (zero nutrient plates and a subset of Murashige and Skoog plates) were quantified using a flame-ionization detector gas chromatograph (Series 15, Dohrmann Envirotech, Santa Clara, CA). A standard curve was developed using serially diluted C2H4 gas. A 1-mL aliquot of plate headspace gases was sampled (through a small hole drilled into the plate's sidewall before pouring media) using a 1-mL syringe and was immediately injected into the gas chromatograph. Measurements were made on the day of germination (d 1), the 2nd d after germination (d 3), and subsequent days until d 7.
NPA was solubilized under alkaline conditions with 1 N NaOH. Aliquots from a sterile-filtered stock solution were added to still molten autoclaved Bacto-agar solutions (final concentrations of 0.1 or 1 µM).
Seedling morphometric measurements were made from Adobe PhotoShop images (600 pixels inch-1; Adobe Systems, Mountain View, CA) captured 7 d after germination by scanning the individual plates on a flatbed scanner. Photomontages of roots were assembled from captured video images (microscope: Diaphot-TMD with a 4x objective, Nikon, Tokyo; black and white camera: SPT M102 CE, Sony, Tokyo) using Scion Frame Grabber (National Institutes of Health, Bethesda, MD). Quantification of root length (distance from base of hypocotyl to root tip), wavelength (distance along root axis between the crests of two successive waves), wave spatial frequency (number of waves per mm of root length), and root axis angle (angle at which a root grew across the agar surface, where vertically down the plate is 0°, toward the right is >0° and toward the left is <0° when viewing the root from above the plate) were measured using the National Institutes of Health Scion Image software program (Windows vBeta 3b; http://www.scioncorp.com). The average root axis angle was measured by tracing the root in the segmented line mode, avoiding those portions of roots that were looping or had penetrated into the medium. Average root elongation was calculated from the increase in root length between d 1 and 7 after germination, and the average temporal wave frequency (number of waves per h) was calculated as the product of elongation rate and spatial wave frequency. All experiments included three replicated plates for each individual treatment (defined by nutrient, Suc, NPA supplements, ethylene injections, or amount of KMnO4 crystals placed in the plate), and experiments were independently repeated at least twice. Seedlings were observed over the 7-d period beyond germination, which usually occurred 2 d after plating.
Scanning electron microscopy micrographs were generated using a Cambridge StereoScan 360 scanning electron microscope equipped with a cryostage. Seedlings were removed from the petri plate, glued to a stub, immediately immersed in liquid nitrogen slush, inserted into the microscope vacuum chamber, etched, gold coated, and photographed at 15 or 20 kV. Composite micrographs were assembled with MicroSoft PowerPoint software (Microsoft, Redmond, WA) and exported as TIFF files.
Upon request, all novel materials described in this publication will be made available in a timely manner for noncommercial research purposes, subject to the requisite permission from any third-party owners of all or parts of the material. Obtaining any permission will be the responsibility of the requestor.
We thank Drs. Jean Yong and Chin Wong and Prof. Haruko Kazama for helpful suggestions and technical assistance; Dr. Jake Jacobsen for use of the flame-ionization detector-gas chromatograph; the Australian National University-Electron Microscopy Unit staff for assistance with the cryoscanning electron microscopy; Dr. Ulrike Mathesius for donation of NPA; and Dr. Gloria Muday for comments on the manuscript. Received December 17, 2002; returned for revision February 21, 2003; accepted March 11, 2003.
Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.102.019182.
1 This work was funded by a Research School of Biological Sciences Strategic Development Initiative Grant (to J.M. and G.O.W.).
[w] The online version of this article contains Web-only data. The supplemental material is available at http://www.plantphysiol.org.
2 Present address: Department of Biology, Wake Forest University, Winston-Salem, NC 27109–7325. * Corresponding author; e-mail masle{at}rsbs.anu.edu.au; fax 61–2–6125–4919.
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) and (
), respectively. Day 1 corresponds to the day of germination. Error bars are SE (n = 12).
2 = 0.0097. Representative phenotypes across the range of conditions are shown, all viewed from above the plate: A, zero salts, 0% (w/v) Suc, and sealed plate; B, zero salts, 0% Suc, and aerated plate; C, Okada and Shimura salts, 0% (w/v) Suc, and sealed plate; and D, Okada and Shimura salts, 0% (w/v) Suc, and aerated plate. The scale bar = 5 mm.
0 µL L-1 on x axis) even after Suc addition. In fact, the most obvious Suc effect on zero-nutrient plates was a decrease in seed germination and retarded seedling development (data not shown). In ethylene-free plates supplemented with Murashige and Skoog or Okada and Shimura nutrients, adding Suc caused a majority of roots to describe a complete circular clockwise loop before penetrating the semisolid medium (
= 9 cm, polystyrene) at 8-mm intervals in two rows 2.5 cm apart onto the medium surface polymerized with 1.5% (w/v) Bacto-agar (Difco Laboratories, Detroit). The medium contained no nutrient supplements ("zero nutrient" plates) or was supplemented with Murashige and Skoog basal salts (M-056 and M-052, Sigma-Aldrich, St. Louis) or the salt formulation used by Okada and Shimura (1990
niewska J, Benková E, Mendgen K, Palme K (2002) Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 415: 806-809
