Journal of Experimental Botany

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Journal of Experimental Botany, Vol. 51, No. 352, pp. 1843-1849, November 1, 2000
© 2000 Oxford University Press

Original Papers

Contrasting effects of ethylene perception and biosynthesis inhibitors on germination and seedling growth of barley (Hordeum vulgare L.)

Jacquiline M. Locke, James H. Bryce and Peter C. Morris¹

Department of Biological Sciences, Heriot-Watt University, Riccarton, Edinburgh EH14 4AS, UK

Received 8 March 2000; Accepted 13 June 2000

	Abstract

Top Abstract Introduction Materials and methods Results Discussion References

 
The effects of the plant growth regulator ethylene, and of ethylene inhibitors, on barley (Hordeum vulgare L.) germination and seedling growth were investigated. Exogenous 1-aminocyclopropane-1-carboxylic acid (ACC) at 100 µM enhanced ethylene production by barley seedlings and stimulated shoot growth, whereas both germination and seedling growth were inhibited by antagonists of ethylene perception (75 µM silver ions, 100 µM 2,5-norbornadiene (NBD)). In contrast, germination was unaffected by, and root and shoot growth of seedlings was strongly stimulated by inhibitors of ethylene biosynthesis (10 µM cobalt chloride, 10 µM aminoethoxyvinylglycine (AVG)). Since the ethylene and polyamine biosynthetic pathways are linked through S-adenosylmethionine, this prompted further explorations into the role of polyamines in germination and seedling growth. Exogenous polyamines (putrescine, spermidine and spermine) at 1 µM concentration stimulated barley seedling growth in a similar fashion to the ethylene biosynthetic inhibitors. Both polyamines and ethylene biosynthetic inhibitors reversed the inhibitory effects of ethylene perception inhibitors on germination and seedling growth. Blocking endogenous ethylene production with aminoethoxyvinylglycine enhanced the free putrescine and spermidine content of germinating barley grains. Thus endogenous polyamines may play a complementary, growth-promotive, role to ethylene in the normal course of barley germination. Further, experiments that have been carried out using inhibitors of ethylene biosynthesis may have to be re-evaluated to take the possible effect of polyamines into account.

Key words: Ethylene, germination, Hordeum vulgare, polyamines.

	Introduction

Top Abstract Introduction Materials and methods Results Discussion References

 
Germination and seedling growth are complex processes in which endogenous plant growth regulators are known to play important and manifold roles (Bewley, 1997). One of these growth regulators is ethylene, which is produced by most plant tissues including germinating seeds and which can have profound effects on the physiology of plants. Exogenous ethylene, or its immediate precursor, 1-aminocyclopropane-1-carboxylic acid (ACC) (Adams and Yang, 1979), will stimulate the germination of many species, and also relieves dormancy in some species (reviewed, Kepczynski and Kepczynska, 1997).

Since the controlled germination of barley is the basis of the malting industry, factors which regulate this process are potentially of great economic importance. There have been some early reports on the effects of ethylene on barley germination which show that ethylene may have a promotive effect on this process (Abeles, 1973). In order to investigate this further, the effects of a stimulant of ethylene production (the ethylene precursor ACC), inhibitors of ethylene perception: silver thiosulphate (Beyer, 1976), and 2,5-norbornadiene, (NBD), (Sisler and Pian, 1973) and inhibitors of ethylene biosynthesis: cobalt chloride which inhibits ACC oxidase (Lau and Yang, 1976), and aminoethoxyvinylglycine (AVG) which inhibits ACC synthase (Amrhein and Wenker, 1979) on barley germination were investigated (Fig. 1). The effects of these compounds on germinating barley show that ethylene plays an important promotive role in barley germination and early seedling growth. However, the contrasting effects of ethylene perception inhibitors and biosynthesis inhibitors prompted the investigation into the effects of another class of endogenous compounds in these processes: the polyamines.

View larger version (30K): [in this window] [in a new window]   Fig. 1. Percentage germination of barley grains after 4 d incubation in the presence of: 100 µM 1-aminocyclopropane-1-carboxylic acid (ACC); 75 µM silver ions (Ag); 100 µM 2,5-norbornadiene (NBD); 10 µM aminoethoxyvinylglycine (AVG); 10 µM cobalt ions (Co). Error bars indicate standard error of the mean.

 

	Materials and methods

Top Abstract Introduction Materials and methods Results Discussion References

 
Plant material
Non-dormant barley (Hordeum vulgare L.) grains of variety ‘Sprite’ were obtained from the 1996 harvest (Hugh Baird and Son Ltd, Pencaitland) and stored at 4 °C. Two replicates of 100 grains were placed on Petri dishes containing the different germination media for each experiment, and left to germinate at 20 °C under a 16/8 h light/dark cycle. After a 4 d period, percentage germination was determined by scoring for radicle emergence, and the root and shoot lengths of 10 randomly picked germinated seedlings from each dish were measured. Germination media were based upon 0.8% (w/v) bacteriological agar in water, buffered with 50 mM MES pH 5.8.

Chemicals
1-Aminocyclopropane-1-carboxylic acid (ACC), dansyl chloride, methylglyoxal bis-guanylhydrazone (MGBG), and cobalt chloride were obtained from Sigma. Bicyclo (2.2.1)-hepta-2,5-diene (2,5-norbornadiene, NBD), 1,4-diaminobutane (putrescine), spermidine trihydrochloride, and spermine tetrahydrochloride were obtained from Fluka. A stock solution of 7.5 mM silver thiosulphate was prepared by a drop-wise addition of a 15 mM solution of silver nitrate to an equal volume of 60 mM sodium thiosulphate solution.

Ethylene and polyamine determinations
Ethylene levels were determined by gas chromatography. Replicate 5 g seedling samples were placed into 15 ml tubes, sealed and left for 2 h at room temperature. Gas samples of 1 ml were fractionated on an alumina F column, 80–100 mesh (Ward et al., 1978). Quantification was by comparison of peak areas to those produced by standard amounts of ethylene.

Free polyamines were extracted in 5% (w/v) HClO₄ as described previously (Flores and Galston, 1982). Samples were then dansylated and analysed by TLC as described earlier (Ye et al., 1997) on Kieselgel 60 plates developed in hexane:ethyl acetate (5:4 v/v). Individual dansylated polyamines were identified by comparison to the R_F of dansylated polyamine standards. The dansylated polyamine bands were scraped off the plate, eluted in ethyl acetate and fluorescence quantified with a spectrophotofluorimeter using an excitation wavelength of 350 nm and a measuring emission wavelength of 495 nm. Polyamine concentrations were determined by reference to known amounts of pure polyamines which had also been dansylated, separated by TLC and eluted from the plate.

	Results

Top Abstract Introduction Materials and methods Results Discussion References

 
Effects of ACC and ethylene inhibitors on germination and seedling growth
Treatment of germinating barley grains with ethylene perception inhibitors repressed both germination percentage and seedling growth; silver thiosulphate at 75 µM or 100 µM NBD decreased germination to about 40% of the control (Fig. 1), and reduced the shoot length of those grains that germinated to approximately half that shown by controls (Fig. 2). Silver thiosulphate inhibited root length to about 30% of the controls, but NBD appeared to have no significant effect on this parameter (Fig. 3). In contrast, the ethylene precursor ACC acted as a stimulant of barley seedling shoot growth; after 4 d germination in the presence of 100 µM ACC shoot length increased (140%) but root length decreased (65%), relative to controls (Figs 2, 3). These results suggest that ethylene is required for optimal germination and growth but, for roots, can be inhibitory to elongation in high amounts, as has been noted in other species (Abeles, 1973).

View larger version (27K): [in this window] [in a new window]   Fig. 2. Shoot length of barley seedlings after 4 d incubation in the presence of: 100 µM 1-aminocyclopropane-1-carboxylic acid (ACC); 75 µM silver ions (Ag); 100 µM 2,5-norbornadiene (NBD); 10 µM aminoethoxyvinylglycine (AVG); 10 µM cobalt ions (Co). Error bars indicate standard error of the mean.

 

View larger version (26K): [in this window] [in a new window]   Fig. 3. Root length of barley seedlings after 4 d incubation in the presence of: 100 µM 1-aminocyclopropane-1-carboxylic acid (ACC); 75 µM silver ions (Ag); 100 µM 2,5-norbornadiene (NBD); 10 µM aminoethoxyvinylglycine (AVG); 10 µM cobalt ions (Co). Error bars indicate standard error of the mean.

 
Paradoxically, and in marked contrast to ethylene perception inhibitors, ethylene biosynthetic inhibitors substantially stimulated seedling growth. Treatment with AVG or cobalt chloride at 10 µM had no negative effect on germination (Fig. 1) and stimulated shoot growth to around 160% of the control plants (Fig. 2). Root length was also enhanced by both AVG (153%) and cobalt chloride (113%) (Fig. 3).

Combined effects of ethylene perception and biosynthetic inhibitors
The inhibition of germination, shoot growth and root growth by the ethylene perception inhibitors (75 µM silver thiosulphate or 100 µM NBD) could be overcome by including additionally either 10 µM AVG or 10 µM cobalt chloride (ethylene biosynthesis inhibitors) in the medium (Figs 1, 2, 3). Germination was restored to close to the control levels by all four perception/biosynthesis inhibitor combinations. Root and shoot length was also increased to levels similar to or greater than those of the control, except for the combination of cobalt chloride and silver thiosulphate, however, these seedlings did have longer roots and shoots than the seedlings treated with silver only.

Effects of polyamines on seedling growth
Since the biosynthetic pathways of ethylene and polyamines are linked through S-adenosylmethione (SAM), the stimulatory effects of the ethylene biosynthetic inhibitors on growth might be due to enhanced polyamine production. Blocking ethylene synthesis will increase SAM flux into other biochemical pathways. SAM can be converted to decarboxylated SAM (dSAM) by the enzyme SAM decarboxylase, and dSAM used for the synthesis of spermidine and spermine.

Hence the effects of exogenous polyamines, alone and in combination with ethylene perception inhibitors, were tested. Inclusion of the polyamines putrescine, spermidine or spermine was not inhibitory to germination and at 1 µM had very similar effects to those of AVG or cobalt in stimulating both root and shoot growth of germinating seedlings to lengths greater than those of the controls (Figs 4, 5, 6). Inclusion of 100 µM MGBG (which competitively inhibits the enzyme SAM decarboxylase and, therefore, should reduce the amount of spermidine and spermine) in the medium slightly reduced germination percentage (88% of the control), shoot length (73% of control length) and root length (92%). The amino acids methionine (precursor to ACC) and arginine (precursor to putrescine) at 1 µM concentration had no significant effect relative to controls (results not shown). Addition of 1 µM putrescine, spermidine or spermine also partially or fully reversed the inhibitory effects of silver thiosulphate or NBD on germination, and stimulated root and shoot growth to levels above those of the control (Figs 4, 5, 6).

View larger version (33K): [in this window] [in a new window]   Fig. 4. Percentage germination of barley grains after 4 d incubation in the presence of: 1 µM putrescine (put); 1 µM spermidine (spd); 1 µM spermine (spm); 100 µM methylglyoxal bis-guanylhydrazone (MGBG); 75 µM silver ions (Ag); 100 µM 2,5-norbornadiene (NBD). Error bars indicate standard error of the mean.

 

View larger version (28K): [in this window] [in a new window]   Fig. 5. Shoot length of barley seedlings after 4 d incubation in the presence of: 1 µM putrescine (put); 1 µM spermidine (spd); 1 µM spermine (spm); 100 µM methylglyoxal bis-guanylhydrazone (MGBG); 75 µM silver ions (Ag); 100 µM 2,5-norbornadiene (NBD). Error bars indicate standard error of the mean.

 

View larger version (29K): [in this window] [in a new window]   Fig. 6. Root length of barley seedlings after 4 d incubation in the presence of: 1 µM putrescine (put); 1 µM spermidine (spd); 1 µM spermine (spm); 100 µM methylglyoxal bis-guanylhydrazone (MGBG); 75 µM silver ions (Ag); 100 µM 2,5-norbornadiene (NBD). Error bars indicate standard error of the mean.

 
The effects of silver ions, AVG and putrescine were determined over a 4 d period of germination (Fig. 7). Silver ions reduced the germination percentage, relative to the control, over the whole 4 d period, but the inclusion of AVG or putrescine with the silver enhanced germination to the control level throughout the time course. Similarly, silver ions reduced root and shoot growth over the 4 d period, but inclusion of AVG or putrescine restored growth back to and above the level of the control.

View larger version (13K): [in this window] [in a new window]   Fig. 7. Shoot length and root length of barley seedlings and percentage germination of barley grains after 2, 3 and 4 d incubation in the presence of 75 µM silver ions, 10 µM AVG, and 1 µM putrescine. () control, (•) silver, () silver+AVG, () silver+putrescine. Error bars indicate standard error of the mean, shown if larger than the symbol.

 

Ethylene and polyamine production by barley seedlings
Ethylene production by 4-d-old germinating barley seedlings was not significantly affected by treatment with either 1 µM polyamines or 100 µM NBD, however, four times more ethylene was generated when barley seedlings were incubated with 100 µM ACC, the immediate precursor to ethylene, and both AVG and cobalt reduced ethylene production to undetectable levels (Fig. 8). Extractable free polyamines were measured in seedlings on days 2, 3 and 4 of germination. In control plants, the levels of putrescine, spermidine and spermine fell by about half by day 4. Treatment with AVG inhibited the decline in putrescine and spermidine levels, but spermine levels showed little or no change as compared to control plants (Fig. 9).

View larger version (12K): [in this window] [in a new window]   Fig. 8. Ethylene production by barley seedlings after 4 d incubation in the presence of: 100 µM 1-aminocyclopropane-1-carboxylic acid (ACC); 10 µM aminoethoxyvinylglycine (AVG); 10 µM cobalt ions (Co); 100 µM 2,5-norbornadiene (NBD); 1 µM putrescine (put); 1 µM spermidine (spd); 1 µM spermine (spm).

 

View larger version (12K): [in this window] [in a new window]   Fig. 9. Extractable free polyamine content of barley seedlings at 2, 3 and 4 d germination in the presence () and absence () of 10 µM AVG. Error bars indicate standard error of the mean.

 

	Discussion

Top Abstract Introduction Materials and methods Results Discussion References

 
These results confirm the importance of ethylene in germination and seedling growth (Kepczynski and Kepczynska, 1997) and show that for barley in particular, this plant growth regulator plays a significant promotive role. Inclusion of ACC in the germination medium (which is converted to ethylene by ACC oxidase, reviewed John, 1997), results in enhanced shoot growth and reduced root growth. In shoots, ethylene is usually associated with an inhibition of stem elongation in both monocotyledonous and dicotyledonous plants. Promotion of seedling shoot growth by ethylene has previously been reported for barley, and also oats and rice (Abeles, 1973). In Arabidopsis, ethylene induces hypocotyl elongation of light-grown seedlings, and inhibits hypocotyl elongation in dark-grown seedlings, suggesting that in seedlings, the response of the shoot to ethylene is light dependent (Smalle et al., 1997).

The inhibition of root growth is a normal characteristic response of plants to high amounts of ethylene (Abeles, 1973); the reason for this is thought to be that mechanical stress results in enhanced ethylene production in the root, and the consequent thickening of the root leads to enhanced mechanical strength (Smalle and Van der Straeten, 1997).

Inhibitor studies require careful interpretation, since any given inhibitor may be non-specific or may not be complete in its intended action. However, two independent inhibitors of ethylene perception that differ in nature, silver ions and NBD, significantly reduced the germination and inhibited the growth of barley seedlings. Silver ions are potent, specific, non-competitive inhibitors of ethylene binding (Beyer, 1976), whereas NBD is a volatile competitive inhibitor of the ethylene receptor (Sisler and Pian, 1973). Using these inhibitors, reductions of germination and growth were not absolute, suggesting either that inhibition of ethylene perception was not 100% or that ethylene is not absolutely required, but significantly enhances these processes.

The results obtained from the experiments with ACC, and with silver ions and NBD, attest to a positive role of ethylene in barley germination and seedling growth. It would be expected that inhibitors of ethylene production would give essentially the same results as inhibitors of ethylene perception. However, as is clear from Figs 1, 2, 3, and 7, both AVG, which inhibits ACC synthase, and cobalt ions which inhibits ACC oxidase, did not impair germination, and enhanced both root and shoot growth beyond that of control plants. No detectable ethylene production was measured from AVG- or cobalt-treated seedlings.

A discrepancy in the reactions of seeds to ethylene perception blockers and biosynthetic inhibitors has been reported previously: AVG and cobalt ions failed to inhibit germination of Amaranthus caudatus, even though exogenous ACC will stimulate germination and NBD will inhibit germination (Kepczynski and Karssen, 1985). Also, NBD will inhibit, but AVG or cobalt do not inhibit the germination of pea seeds (Petruzzelli et al., 1995).

A significant finding was that cobalt and AVG would overcome the inhibitory effects of silver ions or NBD on germination and growth (Figs 1, 2, 3, 7). Thus it appears that under these conditions, ethylene is not a prerequisite for optimal germination or growth since here, ethylene is neither made nor perceived. However, there must be something which is substituting for ethylene. Given that the ethylene and polyamine biosynthetic pathways are linked through SAM, it seemed possible that AVG and cobalt ions may be enhancing polyamine levels by channelling SAM toward the polyamine biosynthetic pathway. It has been shown that AVG treatment will increase spermidine production in orange peel (Even-Chen et al., 1982), and enhanced polyamine levels have been measured in seeds of Cicer arietinum after treatment with cobalt ions and AVG (Derueda et al., 1994).

Free polyamine levels were determined in germinating barley grains and indeed higher levels of polyamines were found in AVG-treated plants after 4 d of germination but curiously, both putrescine and spermidine levels were significantly higher, but not spermine. Higher spermidine and spermine, but not higher putrescine, levels would have been predicted from the biosynthetic pathways; this rebuts the hypothesis that AVG enhances polyamines in barley through an increase in the flux of SAM through the polyamine biosynthetic pathway. A similar finding was made by Kumar et al. when they over-expressed a SAM decarboxylase gene in potato (Kumar et al., 1996); they found enhanced levels of putrescine as well as of spermidine and spermine. This is possibly a reflection of our lack of understanding of polyamine biosynthesis: a complex web of feedback inhibition is described with negative control of ethylene biosynthesis and SAM decarboxylase action by spermine and spermidine, and negative control of arginine decarboxylase and SAM decarboxylase action by ethylene (Evans and Malmberg, 1989; Tiburcio et al., 1997). The increase in putrescine seen in AVG-treated plants may be an indirect consequence caused by disturbing an, as yet, undescribed biosynthetic feedback loop.

Another factor to consider is that AVG may be an inhibitor of many pyridoxal-phosphate-mediated enzyme reactions, and therefore might not only inhibit ACC synthase but also other enzymes (Matoo et al., 1979; Yang and Hoffman, 1984). However, since both ornithine decarboxylase and arginine decarboxylase are themselves pyridoxal enzymes (Sandmeier et al., 1994), it is unlikely that AVG is enhancing putrescine levels in this fashion. Furthermore, the increase in seedling growth was seen with both AVG and cobalt ions, and cobalt is not a pyridoxal enzyme inhibitor.

If the increase in putrescine is responsible for the effect of AVG on growth, it would be expected that exogenously applied polyamines would have similar effects to AVG and cobalt ions on germination and growth. This was the case for putrescine, spermidine and spermine at 1 µM (Figs 4, 5, 6, 7). The polyamines were not simply acting as a nutritional source since they were present at very low levels and similar levels of the amino acids methionine or arginine were without effect. Inclusion of the competitive SAM decarboxylase inhibitor MGBG slightly decreased germination and seedling growth, but since putrescine biosynthesis is not affected by this compound, complete growth inhibition would not be predicted. Exogenous polyamines also overcame the inhibitory effects of silver ions and NBD on germination and growth. These results would support the argument that the stimulatory effects of AVG and cobalt on growth are due to the enhanced endogenous polyamine levels.

The results presented here highlight novel interactions between ethylene, polyamines and plant growth. Firstly, exogenous polyamines are highly stimulatory to seedling root and shoot growth at concentrations of 1 µM. Most previous experiments on the biological effects of polyamines have used millimolar concentrations (Evans and Malmberg, 1989). Secondly, polyamines can substitute for ethylene in the promotion of germination and growth, since they are stimulatory even in the presence of silver ions or NBD. This suggests that both ethylene and polyamines may play complementary roles in regulating early seedling growth. Thirdly, prevention of ethylene biosynthesis by enzyme inhibitors can lead to enhanced endogenous polyamine levels, which may substitute for ethylene in some physiological processes. This may mean that experiments carried out with inhibitors of ethylene biosynthesis may have to be re-evaluated to take the possible effects of polyamines into account.

	Acknowledgments

 
This research was funded by the CK Marr Educational Trust.

	Notes

 
¹ To whom correspondence should be addressed. Fax: +44 131 451 3009. E-mail: P.C.Morris{at}hw.ac.uk

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