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ISSN 1021-4437, Russian Journal of Plant Physiology, 2009, Vol. 56, No. 4, pp. 488–494. © Pleiades Publishing, Ltd., 2009. Published in Russian in Fiziologiya Rastenii, 2009, Vol. 56, No. 4, pp. 539–545.

RESEARCH PAPERS

Response of Maize Seedling Roots to Changing Ethylene Concentrations1 M. V. Alarcona,b, P. G. Lloreta, D. J. Iglesiasc, M. Talonc, and J. Salguerod a

Departamento de Anatomia, Biologia Celular y Zoologia, Facultad de Ciencias, Universidad de Extremadura, Badajoz, Spain b Departamento de Hortofruticultura, Centro de Investigacion “La Orden-Valdesequera”, Badajoz, Spain c Departamento de Genomica y Postcosecha, Instituto Valenciano de Investigaciones Agrarias, Valencia, Spain d Departamento de Biologia Vegetal, Ecologia y Ciencias de la Tierra, Universidad de Extremadura, E-06071, Badajoz, Spain fax 924-28-6201; e-mail: [email protected] Receved April 11, 2008

Abstract—Maize roots (Zea mays, cv. DK 626) growing in aerated solutions showed striking variations in the amount of ethylene produced during different stages of development. As endogenous ethylene increases, root elongation decreases. Exogenous 1-aminocyclopropane-1-carboxylic acid (ACC) supplied to these roots also inhibited their elongation and increased both the fresh weight of the apex and the ethylene produced. The inhibitor of ethylene biosynthesis, 2-aminoethoxyvinyl glycine (AVG), and the inhibitor of ethylene action, silver thiosulfate (STS), also reduced growth and increased swelling. As growth diminishes at reduced ethylene concentrations or with impeded ethylene action, these results support the view that ethylene is necessary for root growth. As ACC treatment also inhibited root elongation, it appears that ethylene was inhibitory at both low and high concentrations. Whereas ACC stimulated ethylene production 4 h after the beginning of treatment, inhibition of root elongation and promotion of fresh weight advanced slowly and needed 24 h to be established. At that time, root elongation reached a maximum response of 60% inhibition and 50% increase in weight. At 48 h, higher doses of ACC were required to provoke the same response as at 24 h. This suggests that the root growth progressively accomodates to higher ethylene concentrations. Key words: Zea mays - root elongation - ethylene inhibitors - ethylene - ACC DOI: 10.1134/S1021443709040074 1

INTRODUCTION Phytohormones greatly affect root growth and development [1-4]. There have been numerous and often contradictory reports concerning the effects of ethylene on root growth. Ethylene tends to be regarded as a regulator of root growth in response to environmental stimuli. In some cases, it has been suggested that ethylene is not the main regulatory factor of root growth and that its action probably occurs only at early stages of development [5]. Nevertheless, there is emerging evidence that ethylene could act in more processes than it was previously thought and even as a root-generated signal [4]. Most experimental studies on ethylene effects on root growth chiefly analyze the response to ethylene after prolonged treatments. To the best of our knowledge, only a limited number of reports refers to the early response of roots to ethylene [6-8]. In long-term 1 This

text was submitted by the authors in English.

Abbreviations: ACC—1-aminocyclopropane-1-carboxylic acid; AVG—2-aminoethoxyvinyl glycine; STS—silver thiosulfate.

(many hours or days) experiments, low concentrations may enhance root elongation, whereas high concentrations inhibit it and simultaneously enlarge root diameter [7, 9]. Ethylene is also involved in a diverse array of cellular, developmental and stress-related processes in plants. A number of examples of the role played by ethylene in the morphogenesis in plants have been described. The ethylene participates, for example, in the control of the formation of reaction wood, floral induction, sex determination, flooding-induced shoot elongation and leaf abscission [10]. At the cellular level, ethylene may be necessary for the formation of a functional root cap [11], controls the differentiation of root hairs [12, 13] and probably regulates the final length attained by root cells [8]. An important research topic concerns the precise role of plant hormones in cell diferentiation. In many instances, it is not clear whether the hormones primarily influence differentiation by early regulating cell fate or by acting during relatively later development. Ethylene action during the differentiation of root hairs

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is a perfect example of this debate. Some genetic and physiological studies clearly implicate to ethylene playing a central role in the developmental of pattern of root epidermis of Arabidopsis. According to Dolan [12] ethylene or its precursor may be a diffusible signal involved in the generation of the spatial pattern of root hairs in Arabidopsis and other plant species. An alternative view suggests that in Arabidopsis the root genes TTG and GL2 are likely to act early to establish cell fate of epidermal cells and to negatively regulate the ethylene and auxin signaling pathways [14]. According to this model, the first event of the differentiation pathway in root hairs would be independent of the the ethylene action. Hence, this hormone would be only related to the promotion of root hair outgrowth once cell-type diferentiation has been initiated. Cho and Cosgrove [15] suggest that two distinctive signaling pathways, one developmental and the other one environmental/hormonal, converge to modulate the initiation of the root hair and the expression of specific expansin gene set. Discussions like this reinforce the interest for analyzing time-course of ethylene action and possible interactions of ethylene with other signals. Evidently, root growth is controlled by interactions between various hormones [16-18]. Particularly interesting for the regulation of root growth are the possible interactions between auxin and ethylene. For example, it has been demonstrated that ethylene decreases polar auxin transport in roots [19]. Consequently, it is possible that ethylene effects on root growth could be mediated by the alteration of auxin concentration in the elongation zone of the root caused by the inhibition of auxin transport. On the other hand, auxin has been considered a positive regulator for ethylene-mediated response in the growth of Arabidopsis roots [20].

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MATERIALS AND METHODS Plant material and growth conditions. Seeds of Zea mays L., cv. DK 626, were surface-sterilized by immersion in ethanol for 5 min. They were then washed three times and soaked in distilled water with aeration at 30°ë. After 24 h, the seedlings with radicles about 1 mm long, were placed vertically in holders made in styrofoam discs and transferred to boxes to be kept in a humid atmosphere and darkness at 30°ë. By 24 h the roots reached a length of 20 ± 5 mm. Discs with 10 selected seedlings of equal root length were placed into bottles containing 1.5 l of well-aerated Hepes buffered growth solution and grown at 30°ë in darkness. Since calcium plays an important role in auxin action in maize roots [25, 26], and potassium is also necessary for root growth [27, 28], the growth medium consisted of a buffered solution of 1 mM Hepes with 1mM CaCl2 and 10 mM KCl at pH 6.0. The ACC, inhibitors, or their combinations were added to the solution after an acclimation period of 24 h, when the roots were 60–80 mm-long. This was designated as zero time in the figures. Measurements and statistical testing. Root length was measured at 4, 24, and 48 h with a ruler (accuracy 1 mm) . Swelling was estimated by measuring fresh weight of apical 10 mm of the roots. The values obtained for these variables are represented as the mean SD of 10 roots. Each experiment was repeated at least twice. Ethylene production was measured in excised apical 10-mm root segments after 4, 24, and 48 h of treatment. Three determinations, each of three segments, were performed for every point. To measure ethylene, the roots were incubated for 1 h in 1-ml vials with 100 µl of the growth solution. After 1h, ethylene was quantified using a gas chromatograph (HP 6890 series) equipped with an activated alumina column and a flame ionization detector. The total amount of ethylene produced during a period was calculated from the ethylene production rates at different times. Each experiment was repeated at least twice.

Ethylene biosynthesis inhibitors have been proved to be good tools to analyze the participation of this phytohormone in diverse physiological processes. The final step of ethylene biosynthesis is the oxidation of the ethylene precursor 1-aminocyclopropane-1-carboxylic acid (ACC) to ethylene. AVG (2-aminoethoxyvinyl glycine) is an ethylene biosynthesis inhibitor precisely because it inhibits the enzyme ACC synthase [21]. The conversion of ACC to ethylene is also inhibited by cobalt ions [22, 23]. The silver ion is another type ethylene inhibitor, because it inhibits ethylene action rather than biosynthesis in a wide variety of ethylene-induced responses [24]. Hence, ethylene inhibitors are good tools to determine what effects are due to ethylene altered concentrations or to lack of response to ethylene.

Chemicals. ACC and AVG were prepared as concentrated solution in 1 mM Hepes buffer. The volumes added were less than 0.1% of the total volume, except for STS where the ratio was 1%. All chemicals were purchased from Sigma (United States) except the CaCl2 and KCl (Merck, Germany).

The aim of the present study was to follow the time course of inhibition of root elongation and increase in fresh weight by ethylene produced from the ethylene precursor ACC in maize seedlings grown in aerated solutions. We also used both the inhibitors of both ethylene biosynthesis and action in order to distinguish root growth at low ethylene concentrations from that with inhibited ethylene action.

Comparison of growth parameters and ethylene production was performed using unplanned multiple comparison tests according to the T-method after a one-way ANOVA analysis [29]. Only differences of means with P ≤ 0.05 were considered to be significant. The linear correlation coefficient of ethylene production with the logarithm of ACC concentration was also calculated in short-term experiments for 4 h.

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20 0 9 Root tip fresh weight, mg

RESULTS Effects of ACC Treatment on Root Elongation, Root Tip Fresh Weight, and Ethylene Production In a first set of experiments we tested the effect of 1, 5, and 10 µM ACC. After the acclimation period, control roots with a length of 60-80 mm grew at a rate of 2.4 ± 0.4 mm/h during the first 24 h, increasing their length by about 58 mm. During the following 24 h, the growth rate declined slightly to 2.0 ± 0.4 mm/h (Fig. 1a). The fresh weight of control root apices decreased and the ethylene production increased significantly at the time when the changes in root growth occurred (Figs. 1b, 1c). While the roots grew from 70 to 180 mm within 48 h, the ethylene production increased fourfold (Fig. 1c), but the parallel decrease in root growth rate was only by 17%, suggesting that major changes in ethylene production occurred necessary before root elongation is significantly affected. Root elongation and fresh weight of root apex showed no apparent change during 4 h of the experimental period (Figs. 1a, 1b). Later, treatments with at least 1 µM ACC for 24 h resulted in completely bent roots growing with negative gravitropism. There was a strinking difference in the growth response of roots to ACC treatments at 24 h, when the production of ethylene was moderate (1.67 ± 0.17 nl/(g fr wt h), and at 48 h, when it increased up to about 4.55 ± 0.20 nl. During the first day of treatment, the ethylene precursor ACC inhibited root elongation and increased fresh weight and ethylene production (Figs. 1a–1c). In general terms, the effect was dependent on ACC concentration in the range of 1.0–10 µM, but the thresholds for the response to ACC in terms of the elongation rate and fresh weight gain were not similar. For example, the inhibition of elongation caused by 1 µM ACC was estimated as 23%, whereas the weight was similar to the control (Fig. 1b). At higher ACC concentrations, the inhibition of root elongation was about 50%, but no complete inhibition was observed even at 10 µM ACC. The weight of 10-mm root tips significantly increased by 44% after 5–10 µM ACC treatments (Fig. 1b). During the second day, the ACC doses required to affect root growth considerably increased, thus indicating an essential modification of ethylene metabolism or sensitivity in the root. The elongation rate was affected by ACC concentrations even up to 1 µM (Fig. 1a), and the weigth increased only after 5 µM and higher ACC treatments (Fig. 1b). Root elongation exhibited a maximum response of 60% inhibition, but there was only a 12% weight gain. The rate of ethylene production was measured three times after ACC additions to determine whether the ACC supplied is metabolized throughout the experimental period and eventually increased ethylene levels in the roots (Fig. 1c). Initially, the ACC treatment increased ethylene production in a concentrationdependent way. Four hours after addition, the ethylene production rates depended linearly on the logarithm of

(b) 8 7 6 3 4 2 1

5 4

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(c) Rate of ethylene evolution, nl/(g fr wt h)

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0

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20 30 40 Time of incubation, h

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Fig. 1. (a) Effect of ACC on elongation of maize roots. ACC concentrations tested were added to the growth solution when roots were 60-70 mm long (time zero). (1) Control roots; (2) treatment with 1 µM ACC; (3) treatment with 5 µM ACC; (4) treatment with 10 µM ACC. (b) Effect of ACC on fresh weight of apical 10 mm of maize roots. (c) Effect of ACC on ethylene production by maize roots. Rates were calculated by using root fresh weight measured after ethylene determination.

the ACC concentration (nl ë2ç4/(g fr wt h) = 28.962 + 3.949 log ACC concentration, r = 0.99). In general, this initial increase in ethylene production appeared to be transitory in the case of low ACC doses: the 1 µM ACCtreated root tips, which at 4 h showed a four-fold increase in ethylene production, after 48 h showed the levels similar to the control roots (Fig. 1c). Neverthe-

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Effects of ethylene inhibitors and ethylene precursor (ACC) on maize root length, fresh weight of root tip and ethylene evolution Treatment

Rate of ë2 H ** 4

Root length*

Fresh weight*

100 ± 10a

100 ± 10a

100 ± 15a

AVG, 1 µå

74 ± 4b

80 ± 9a

13 ± 1b

STS, 100 µå

101 ± 8a

85 ± 6a

54 ± 4c

Control

evolution

ACC, 1 µå

72 ± 10b

93 ± 3a

199 ± 13d

ACC, 5 µå

38 ± 8c

125 ± 11b

650 ± 76e

ACC, 5 µå + STS, 100 µå

98 ±

91 ±

80a

657 ± 47e

5a

Different letters indicate significant differences at P < 0.05. Notes: Results are presented as % of control. Different letters designate differences significant at P < 0.05. * Measured in 24 h. ** Measured during the period from 4 to 24 h.

less, roots treated with at least 5 µM ACC, that initially ten-fold increased their ethylene production or even more over the controls, despite a decline still produced more ethylene than control roots after 48 h (Fig. 1c). The time-course of the response of maize roots to ACC treatments should be considered in the context of changing endogenous ethylene concentrations. There was an initial strong increase in ethylene produced at 4 h in response to exogenous ACC which did not result in efficient growth alterations. This peak coincided with slowly rising endogenous ethylene levels in control roots (Fig. 1c). As ethylene levels rose, both endogenous and exogenous, for 24 h, root elongation progressively decreased and root tip weight increased. Finally, at 48 h when endogenous ethylene levels are the highest, the amount of ethylene produced in response to ACC treatment decreased. This indicates that exogenous ACC becomes less efficiently converted to ethylene at this time. One-Day Treatments with Ethylene Inhibitors Preliminary experiments demonstrated that both ethylene inhibitors, AVG (inhibitor of ACC synthase) and STS (inhibitor of ethylene action) do not affect root elongation after 4-h-long treatment (data not shown). For this reason we measured the weight of root tips only after a 24-h incubation in inhibitor solutions. Elongation and ethylene production were measured within 4–24 h in the presence of inhibitors. STS was used alone or in combination with 5 µM ACC. Treatment with AVG for 24 h decreased root elongation but did not promote significantly the root swelling measured as fresh weight increase (table). The total ethylene produced during 4–24 h by root tips was reduced significantly by AVG to about 13% of the control value (table), indicating that AVG really inhibited ethylene biosynthesis. After 24 h of AVG treatment, ethylene production was not detectable due to total inhibition of RUSSIAN JOURNAL OF PLANT PHYSIOLOGY

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ethylene biosynthesis. The ethylene action inhibitor STS at 100 µM concentration did not significantly modify either root elongation or tip weight (table), but ethylene production was reduced to 54% of control value. Treatment with 1 µM ACC two-fold increased ethylene production rate and reduced significantly elongation by about 72% as compared to untreated roots, but did not no modified the weight of root tips. These results indicated that elongation is more sensitive than swelling to changes in ethylene levels. As previously demonstrated, 5 µM ACC added to the growth solution reduced root elongation, increased weight, and enhanced ethylene production (Figs. 1a–1c, table). The effects on maize root growth could be due to a direct action of ACC or, more probably, to the increased ethylene concentration produced after ACC treatment. To demonstrate that these effects were caused by the conversion of exogenous ACC to ethylene, we analyzed what happened with roots simultaneosly treated with ACC and STS. Under these conditions, the effects of ACC on root elongation and apex weight were completely reversed (table) without any modification of ethylene production. DISCUSSION Ethylene has long been recognized as a phytohormone that regulates root growth, particularly in roots growing under mechanical impedance or other root stresses [1, 11, 30]. Increase in ethylene production and reduction of root length were reported in maize roots [31]. The ethylene production rates in our experiments are similar to [31]. However, there is no common opinion about the relative importance of ethylene in regulating unstressed root growth. Ethylene is known to inhibit root elongation in maize [7], Arabidopsis thaliana [32, 33], and Pisum sativum [34, 35]. Rodrigues-Pousada et al. [36] demonstrated that, during the No. 4

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initial development of Arabidopsis seedlings, an ACC synthase gene was expressed to play a role in the development of both root and shoot systems. If ethylene inhibits unstressed root growth, one would expect some ethylene-insensitive mutants to show altered growth. However, a recent study of tomato ethylene-insensitive mutant (never ripe) demonstrated that root development was actually anomalous when roots grew in sand (impeded), but normal when roots were in nonimpeding potting medium [37]. Our results support the view that ethylene is necessary for root growth, but at the same time an excess of ethylene can inhibit this process. Ethylene is necessary for root growth because both ethylene inhibitors reduced root elongation, some being more effective than others, but all acting in the same direction. Decreased elongation was apparent 24 h after inhibitor treatment. Therefore, very low levels of ethylene are sufficient to initially support normal root development, and only when the ethylene levels decline below a critical value the elongation began to diminish. Excessive ethylene diminishes root elongation, as follows from the finding that ACC treatments enhanced ethylene production and inhibited root elongation (Figs. 1a, 1b). Consequently, for root growth both deficiency and excess of ethylene are inhibitory. Nevertheless, the moderate variations in root growth promoted by various produced ethylene concentrations suggest that the range of ethylene concentrations supporting adequate growth is rather wide. For this reason we may conclude that ethylene is more involved in the fine-tuning rather than in the general control of root growth. Ethylene controls the elongation in Arabidopsis roots by regulating both the oxidative crosslinking of hydroxyproline-rich glycoproteins and the callose deposition in the root cell walls in the elongation zone [8]. Ethylene is also known to initiate a fascinating signaling pathway via four main modules, namely, phosphotransfer relay, an EIN2-based unit, a ubiquitin-mediated protein degradation component, and a transcriptional cascade [38]. In Zea mays root, consistent swelling measured as root-tip weight gain occurred at least after 5 µM ACC treatment. Ethylene has been implicated as the main effector of root transversal expansion in dicot species [18, 39]. In our experiments, ACC was highly efficient in increasing ethylene biosynthesis but not so effective in inducing root swelling. Most our observations suggest that the treatments which enhance root elongation inhibit root swelling and vice versa, so that these two processes appear to be inversely related. Indeed, inhibited elongation and transverse expansion are two manifestations of the classical triple response phenotype that plants show being exposed to an excess of ethylene [40]. Nevertheless, this correlation is not general. For example, in Ranunculus scleratus petioles cell elongation can be separated from radial expansion, the former process being regulated mainly by ethylene and gibberellic acid, and the latter by auxin [41].

The time-course of the response of maize roots to changing ethylene concentrations has interesting implications. The reports in the literature are limited in number and frequently contradictory. In segments of pea root, Chadwick and Burg [34] observed that the stimulation of ethylene biosynthesis by auxin was maintained for 24 h, and concluded that ethylene is the normal mediator in the inhibition of root elongation by auxin; i.e., that the effect of auxin on elongation is due to the ethylene produced in response to the auxin. However, Eliasson et al. [35], using the same plant material and auxin concentration, found an initial stimulation of ethylene biosynthesis by auxin, but similar ethylene production to controls 24 h after the auxin treatment. Therefore, they proposed that the inhibitory effect of auxin is not caused by ethylene. We here found that at 4 h, although ethylene levels are increased, the elongation is not inhibited. This indicates that the response of the maize root to ethylene needs several hours to be fully established. The finding, that at 48 h the ACC concentrations required to stimulate root growth increased considerably, suggests that the sensitivity to exogenous ACC treatments is diminished when the levels of endogenous ethylene production are high. In this case, perhaps the root has naturally adapted to the high ethylene levels. Finally, some interactions between ethylene and other phytohormones may regulate root growth. It is well known that auxin promotes ethylene biosynthesis [34]. However, the opposite effect that ethylene promotes auxin biosynthesis, might also be true because it was recently demonstrated that ethylene regulates the expresion of WEI2 and WEI, i.e., two genes encoding subunits of the anthranilate synthase, a rate-limiting enzyme in triptophan biosynthesis [42]. Ethylene not only stimulates auxin biosynthesis but also regulates the expression of several PIN auxin-efflux components and a PIN auxin influx carrier by a direct or indirect mechanism finally affecting the auxin transport [43]. Auxin is probably the main regulator of root growth and plays a positive regulator role in the ethylene response [20]. Nevertheless, an adequate concentration of endogenous ethylene is also neccesary for root growth. ACKNOWLEDGMENTS This work was supported by grants IPR98B016 and 2PR01B009 from the Consejeria de Educacion y Juventud (Direccion General de Ensenanzas Universitarias e Investigacion) de la Junta de Extremadura. REFERENCES 1. Feldman, L.J., Regulation of Root Development, Annu. Rev. Plant Physiol., 1984, vol. 35, pp. 223–242. 2. Klee, H. and Estelle, M., Molecular Genetic Approaches to Plant Hormone Biology, Annu. Rev. Plant Physiol. Plant Mol. Biol., 1991, vol. 42, pp. 529–551.

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