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First published online March 26, 2004; 10.1104/pp.103.031088 Plant Physiology 134:1614-1623 (2004) © 2004 American Society of Plant Biologists Transient Exposure to Ethylene Stimulates Cell Division and Alters the Fate and Polarity of Hypocotyl Epidermal Cells1Department of Biology, International Christian University, Mitaka, Tokyo 181–8585, Japan (H.K., H.D.); Plant Cell Biology Group, Research School of Biological Sciences, The Australian National University, Canberra, Australian Capital Territory 2601, Australia (H.K., G.O.W.); School of Agricultural Sciences, Nagoya University, Chikusa, Nagoya 464–8601, Japan (H.I.); and Department of Botany, University of British Columbia, Vancouver, British Columbia, Canada V6T 1Z4 (G.O.W.)
After transient exposure to the gaseous hormone ethylene, dark-grown cucumber (Cucumis sativus) hypocotyls developed unusual features. Upon ethylene's removal, the developing epidermis showed significant increases in cell division rates, producing an abundance of guard cells and trichomes. These responses to ethylene depended on the stage of development at the time of ethylene exposure. In the upper region of the hypocotyl, where cells were least differentiated at the onset of ethylene treatment, complex, multicellular protuberances formed. Further down the hypocotyl, where stomata and trichomes were beginning to develop at the onset of ethylene exposure, an increase in the number of stomata and trichomes was observed. Stomatal complexes developing after the ethylene treatment had a significant increase in the number of stomatal subsidiary cells and the number of cells per trichome increased. Analysis of division patterns in stomatal complexes indicated that exposure to ethylene either suspended or altered cell fate. Ethylene also altered cell division polarity, resulting in aberrant stomatal complexes and branched trichomes. To our knowledge, the results of this study demonstrate for the first time that transient treatment with physiological concentrations of ethylene can alter cell fate and increase the propensity of cells to divide.
Ethylene regulates a variety of physiological and biochemical processes in plants, such as fruit ripening, senescence, abscission, sex determination, root initiation, and cell elongation (Abeles et al., 1992  ). Ethylene also regulates the size and stature of plants in response to various environmental cues (Abeles, 1973; Kieber, 1997). Its effects on dark-grown seedling development, described initially as the triple response, include increased radial growth of the root and stem, reduced root and stem elongation, and abnormal horizontal stem growth (Neljubow, 1901; Knight et al., 1910). The term triple response, as it is now commonly used, includes exaggeration in the curvature of the apical hook instead of abnormal horizontal growth (Bleecker et al., 1988; Guzman and Ecker, 1990 and references therein). The triple response of Arabidopsis has been exploited for characterizing the ethylene signal transduction system by identifying numerous mutants that either phenocopy the triple response in the absence of exogenous ethylene or fail to respond properly to ethylene (Guzman and Ecker, 1990).
The dramatic stimulation of radial swelling of stems and roots by ethylene has led to physiological studies and cellular analyses of this phenomenon (Burg and Burg, 1966
In contrast to numerous studies of ethylene's effects on organ expansion, very few studies have considered ethylene's effects on cell division. As seedling growth accompanies cell division in the apical meristem, suppression of seedling growth by ethylene implies that the gaseous hormone inhibits both cell elongation and division. Inhibition of DNA synthesis by ethylene was reported in meristems of shoots and roots of pea (Pisum sativum; Burg and Burg, 1968 In this study, we examined how ethylene treatments alter cell division patterns in the progenitors of guard cells and trichomes of etiolated seedlings of cucumber (Cucumis sativus). We document for the first time to our knowledge that after exposure to ethylene at levels likely to be encountered during bouts of stress, cell division polarity is altered and that there is an increased propensity for cell division, organogenesis, and histogenesis.
Most of ethylene's known effects on plant development have been observed during continuous ethylene treatments. We wanted to examine the consequence of transient exposure to ethylene, and therefore documented the structural changes that took place following exposure to exogenous ethylene. We chose the hypocotyl because it provides a range of developmental stages, with differentiation progressing from the base upwards. In hypocotyls, postembryonic division is confined to cells that give rise to stomatal complexes and trichomes so it is possible to quantify changes in cell division that are dependent on a given treatment.
We first examined the effects of ethylene on stomatal development along the entire length of the hypocotyl. We grew seedlings in the dark in airtight containers throughout the treatment period. Three days after planting in normal air, we injected 10 µL L–1 ethylene into the containers and after 2 d, ventilated them to restore normal air for a further 2 d. Control seedlings were grown continuously in the containers and injected with normal air and ventilated at the same times as the ethylene-treated seedlings. Compared to untreated seedlings (Fig. 1A
), ethylene-treated seedlings had relatively short hypocotyls, approximately 70 to 85 mm in length (Fig. 1B). During the 2-d ethylene treatment, cell growth was greatest in the lower mid region (Fig. 1B, zone 3), which consequently underwent radial expansion over the course of exposure to ethylene. Stomatal development progresses apically from the base of the hypocotyl, which can be divided into four developmental zones (Table I). It is known from a previous study (Kazama and Mineyuki, 1997
Snorkel-Like Protuberances Form in the Region with Greatest Development Potential Once ethylene was removed from the containers, the upper region of the hypocotyl (Fig. 1B, zones 1 and 2) continued elongating with no apparent radial swelling. Within 2 d of removing ethylene, conspicuous protuberances developed in the uppermost (apical) zone (Fig. 1B, zone 1; Fig. 2, A and B ). Scanning electron micrographs of the protuberances revealed that they always terminated with at least one stoma (Fig. 2A) and commonly developed trichomes (Fig. 2B). Protuberances ranged from 20 to several thousand cells in size. In some experiments we achieved a sustained release of ethylene over longer periods of time (up to 7 d) by enclosing a ripe apple (Malus domestica) within the container from the time of seed planting (Fig. 2D). In these cases the protuberances were generally larger than those produced after the 2-d pure ethylene exposure. Unlike adventitious roots, which commonly develop in dark-grown cucumber hypocotyls under high humidity (Fig. 2C), protuberances showed no discontinuity with the surrounding epidermis and cortex tissues (Fig. 2, D and E). Air-filled cavities were detected during the early stages of protuberance development (Fig. 2F). Notably, the longer ethylene treatments using a ripe apple also resulted in large cavities in the center of the hypocotyl (Fig. 2D), though these cavities may have been present before removing the apple. We also observed analogous structures in the upper regions of Arabidopsis hypocotyls after seedlings were exposed to ethylene during the early stages of development (Fig. 2G). The phenomenon is therefore not a peculiarity of cucumber seedlings.
In the upper midzone (Fig. 1B, zone 2), where guard mother cell commitment was taking place at the time of ethylene exposure, protuberances did not form, but the number of stomata was increased significantly. To quantify this effect, we measured stomatal frequency (defined as the number of stomata for every 100 epidermal cells; Kazama and Mineyuki, 1997
In addition to the increased incidence of stomata, exposure to ethylene increased the number of nonspecialized epidermal cells in the stomatogenesis-competent zones. The pattern of stomatogenesis in light- and dark-grown seedlings is compared schematically in Figure 3 . Stomata developing in normal air in the dark consist on average of a pair of guard cells subtended by one undivided subsidiary mother cell, which was the sister cell of the original guard mother cell (Figs. 3 and 4A ). By comparison, 5 to 10 subsidiary cells surround each stoma in light-grown seedlings (Fig. 3). After transient ethylene treatment, however, we detected many extra cells adjacent to guard cells, especially in the upper and lower midzones (Fig. 1B, zones 2 and 3; Fig. 4, B–D). The mean number of cells in stomatal complexes, including guard and other epidermal cells, was 12 (n = 30–50 for three separate experiments) in the dark-grown seedlings, more than the usual number of subsidiary cells found in light-grown seedlings. Nearest the hypocotyl base (Fig. 1B, zone 4), stomata were found in normal abundance but some guard cells, distinguished by their morphology and chloroplasts, had undergone extra divisions (Fig. 4K).
We detected a high proportion of unusual and defective stomata in the upper midzone (Fig. 1B, zone 2), and to a lesser extent, in the lower midzone (zone 3). Stomatal twins (Fig. 4, E and F) were very common, suggesting that processes inhibiting the formation of adjacent stomata were perturbed by ethylene. Guard cell division planes were also frequently aberrant in the midzones (Fig. 1B, zones 2 and 3; Fig. 4, G–J). Figure 4G shows two oppositely oriented stomata, formed as a result of extra transverse divisions of the stomatal progenitor cell. In some cases, the normally longitudinal guard mother cell division planes (Fig. 4A) were transverse (Fig. 4H), oblique (Fig. 4I), or even periclinal (Fig. 4J). Quantitative analysis showed that while stomata were consistently oriented almost parallel to the longitudinal axis in the seedlings grown without exogenous ethylene (Fig. 5A ), stomatal orientation deviated greatly from the longitudinal axis in seedlings exposed to ethylene (Fig. 5B).
Ethylene Exposure Stimulates Extra Cell Numbers and Branching in Trichomes Trichome formation, like stomatogenesis, is a feature of postembryo hypocotyl development that involves cell division. Under normal conditions, trichomes develop either as hair-form or secretory trichomes. The hair-form trichomes point downward and terminate with a fourth cone-shaped cell (Figs. 6A and 7A ). Secretory trichomes are much smaller and point toward the top of the hypocotyl, with a three-celled stalk and a four-celled globular head (Fig. 7B).
To determine ethylene's effects on trichome development, we examined trichomes after exposing dark-grown seedlings to ethylene at a range of concentrations from 0.1 to 300 µL L–1 for 24 h on day 3. Transient ethylene exposure stimulated trichome formation, increased the number of cells per trichome, stimulated trichome branching, and altered the fate of trichomes to specialize as secretory or nonsecretory trichomes. In untreated control seedlings, hair-form trichomes had a maximum of four cells (Fig. 6A), whereas seedlings that had been exposed to 100 µL L–1 ethylene had hair-form trichomes consisting of as many as seven cells (Fig. 6, B and C). The mean number of cells per trichome after ethylene treatment was apparently only moderately higher than in the control treatments, but this statistic reflects the fact that the total population of trichomes also included many two- and three-celled immature trichomes, whose formation was also initiated after ethylene treatment (Fig. 6, B and C). The mean number of cells per trichome increased in proportion to the concentration of ethylene applied within the range of 0.1 µL L–1 to 100 µL L–1 (Fig. 6D). The correlation factor of the dose response curve was R = 0.99, indicating that the increase in trichome cell number was dependent on ethylene concentration. Branching of trichomes was observed in 38.2% of the trichomes (n = 386) of seedlings exposed to ethylene (10 µL L–1) for 48 h following 2-d incubation in normal air (Fig. 6E). No branched trichomes were detected in control seedlings. Transient ethylene treatment resulted in a range of unusual trichomes. Some secretory trichomes developed with extra cells, either in the stalk (Fig. 7C) or head region (Fig. 7D). In other cases, trichomes were of mixed character, including downward-bending secretory trichomes (Fig. 7E), upward-bending hair-form trichomes (Fig. 7D), and trichomes with both globular heads and cone-shaped end cells (Fig. 7F).
To date, most ethylene research has focused on the effects of ethylene on gross morphology during continuous application. In contrast, our study examined the consequences of seedling development to short-term ethylene exposure, which simulates ethylene signaling in plants as they respond to many environmental signals and stresses, which are often transient.
Our study looked beyond seedling morphology to examine how short-term ethylene exposure alters cell differentiation patterns. The hypocotyl epidermis is ideal for this because the only postembryonic divisions are those giving rise to stomata and trichomes. Hypocotyl development, which includes epidermal cell expansion as well as the differentiation of stomata and trichomes, begins at the base and progresses toward the cotyledons (Kazama and Mineyuki, 1997 The results of our study demonstrate that ethylene exposure has considerable promotive effects on cell development that are only manifested after the initial signal subsides. These effects differ dramatically from the responses of cells during ethylene exposure. They include increased propensity for cells to divide, altered cell fate and altered division polarity. These three effects are now discussed.
In a companion study, we report that continuous ethylene treatment suppresses cell division but that removing ethylene triggers an exceptional burst of cell division activity (Dan et al., 2003
Ethylene also promotes rapid stem elongation and adventitious root formation in submerged amphibious plants. In deepwater rice (Oryza sativa), apparent stimulation of cell division by ethylene has also been reported (Métraux and Kende, 1984
Our results show that ethylene extends the period during which cells remain competent for division. As a result, cells that would normally cease dividing instead retain the capacity for further rounds of division upon removal of the ethylene block. It is well known that continuous exposure to auxin and cytokinin stimulates proliferation of plant tissues (den Boer and Murray, 2000
Could altered cell to cell signaling during ethylene exposure account for the apparent developmental regression of cells? Asymmetric division of the progenitors of guard mother cells in dicot leaves is considered to be crucial for subsequent differentiation into guard mother, subsidiary, and guard cells (Zhao and Sack, 1999
Stomatal patterning in Arabidopsis hypocotyls is, like root hairs, highly dependent on cell positioning (Berger et al., 1998
Transient ethylene exposure also altered division planes, and generated aberrant stomatal complexes and branched trichomes. Interestingly, transient red light exposure to otherwise dark-grown seedlings can also produce aberrant stomata (Kazama and Mineyuki, 1997
Our results show that ethylene signaling impinges on the mechanisms that control division planes and tissue patterning. Mutational approaches are beginning to identify elements that control these processes (Otegui and Staehelin, 2000
The formation of protuberances in the upper zone of cucumber hypocotyls is compelling evidence that ethylene not only stimulates proliferation and alters cell fate but may also play a pivotal role in the direction of organ development. The protuberances form at right angles to the hypocotyl growth axis, suggesting that a new growth polarity is established in the presence of ethylene. Hypocotyl protuberances can also be stimulated when carrot (Daucus carota) seedlings are agitated in the presence of abscisic acid (ABA) and, when agitation ceases, these eventually develop into somatic embryos (Nishiwaki et al., 2000
The protuberances, which always form with stomata at their tips, are reminiscent of ray parenchyma, whose frequency and development in woody tissues are stimulated by ethylene. According to the ethylene aeration hypothesis, the centrifugal flow of ethylene through ray initials promotes the differentiation of vascular rays in radial directions (Lev-Yadun and Aloni, 1995 Finally, one simple explanation for the very rapid responses observed is that the expression of ethylene receptors is up-regulated during ethylene exposure. Removal of ethylene gas from the experimental containers would result in an unusually large proportion of unbound ethylene receptors, creating a state that could counteract the generally negative effects ethylene has on normal development. Investigating this possibility and the other novel phenomena described in this study should pave the way for identifying new aspects of ethylene physiology, and impinge on future strategies to identify new sensory, regulatory, and transcription factors in ethylene signaling.
Plant Materials and Growth Conditions
Cucumber (Cucumis sativus) L. cv Aonagajibai seeds purchased from Takii Seed (Kyoto) were imbibed for 2 h and planted in Smithers-Oasis growing medium (nutrient free medium, H–TC276, Nippon Soda, Tokyo) or in 0.35% (w/v) plain agar medium (Bacto-agar, DIFCO Laboratories, Detroit), and grown at 25°C ± 1°C in total darkness unless otherwise mentioned. Two different growth cabinets were used (Koitotron KG206, Koito Industries, Tokyo, or a Sherer CEL15 cabinet, Sherer-Pennant, Seven Hill, Australia) with no difference in results. For ethylene treatments and controls, seedlings were cultured in 825-ml glass, airtight containers whose acrylic lids were drilled to accommodate gas chromatography-grade silicon plugs (Shimazu, Kyoto). Four seedlings were grown in each container. Three days after germination, reagent-grade ethylene (Nippon Sanso, Tokyo) was injected through the plug using a hypodermic syringe. Equivalent volumes of normal air were injected for control treatments. Gas chromatograph mass spectrometric analysis demonstrated that ethylene levels were steady over at least 7 d after a single injection (data not shown). A small block of ice was placed on top of the lid to facilitate circulation of gas within the container. For experiments requiring a sustained release of ethylene over a long term, a ripe apple, expected to release between 10 and 50 µL L–1 ethylene, was placed inside a 20-L airtight acrylic container at time of planting. For experiments investigating trichomes, seedlings were exposed to red light for 30 min on day 2 to induce trichome development. For quantitative analysis, each experiment was repeated at least 10 times. All other treatments were repeated at least three times. Arabidopsis seedlings were grown in petri dishes as described (Sugimoto et al., 2000
For morphological studies, epidermal strips were peeled from the hypocotyl with fine forceps. Microscopic observations were performed with an Olympus microscope (New Vanox S AHBS-s, Olympus, Tokyo) equipped with DIC optics.
Hypocotyl segments were attached to mounting plates with a 50:50 mixture of Tissue-Tek tissue freezing medium (Miles Scientific, Naperville, IL) and colloidal graphite (Agar Aids, Stansted, Essex, United Kingdom) and rapidly frozen by plunging them into liquid nitrogen slush at –230°C. The plate with attached sample was then inserted into the preparation chamber of an Oxford CT1500 Cryo Preparation System and slowly warmed to –80°C to sublimate ice crystals from the specimen surface. The cryochamber temperature was adjusted to –169°C and, by introducing a plasma of argon gas to the chamber, the specimen was sputter-coated with 100 Å gold particles for approximately 3 min, resulting in a 10-nm coating. The frozen sample was then transferred to a cryo stage at –185°C, which fitted inside the chamber of a Cambridge Instruments S360 scanning electron microscope (SEM). The electron optics system of the SEM was optimized for high resolution, but with sufficient depth-of-field to enable the entire object to be focused. This involved the use of a final aperture, 30 µm in diameter, a working distance of approximately 18 mm, electron beam current of 80 pA and an accelerating voltage of 15 kV. The sample was maintained at approximately –165°C throughout the SEM viewing operation. Images were recorded electronically as TIF files and as photographic negatives on Kodak PXP 6057 black and white film.
To view newly formed cell walls in stomatal complexes and in trichomes, freshly peeled epidermal strips were incubated with 0.05% (w/v) aniline blue (Schmidt gmbH, Keonigen, Netherlands) in phosphate-buffered saline buffer at pH 8.5. After 5 min incubation in the dark, fluorescence microscopic observation was performed under violet light irradiation with an Olympus microscope (New Vanox S AHBS-s, Olympus). Images were recorded on photographic negatives on Fujicolor Superia 400 film (Fuji Photo Film, Tokyo). The angular deviation of the cell division plane from the normal longitudinal orientation was measured on digitized images using the public domain NIH Image program (developed at the United States National Institutes of Health and available on the Internet at http://rsb.info.nih.gov/nih-image). 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 permissions will be the responsibility of the requestor.
We thank Prof. B.E. Gunning for valuable suggestions, Dr. M.E. Galway for critical reading of the manuscript, and Dr. R. Heady from the Australian National University Electron Microscopy Unit for excellent technical assistance with the SEM. Received July 30, 2003; returned for revision October 1, 2003; accepted January 3, 2004.
1 This work was supported by a grant in aid from the Ministry of Education, Science and Culture, Japan (grant no. 11874120 to H.K.), and by the Australian Research Council Discovery Project (grant no. DP0208872 to G.O.W.).  Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.103.031088 * Corresponding author; e-mail kazama{at}icu.ac.jp; fax 81–(0)422–331449.
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