JXB Advance Access originally published online on July 2, 2004
Journal of Experimental Botany 2004 55(404):1821-1830; doi:10.1093/jxb/erh187
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RESEARCH PAPER |
Impact of pedospheric and atmospheric sulphur nutrition on sulphur metabolism of Allium cepa L., a species with a potential sink capacity for secondary sulphur compounds
Laboratory of Plant Physiology, University of Groningen, PO Box 14, 9750 AA Haren, The Netherlands
* To whom correspondence should be addressed. Fax: +31 50 363 2273. E-mail: l.j.de.kok{at}biol.rug.nl
Received 18 February 2004; Accepted 29 April 2004
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Abstract |
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Onion (Allium cepa L.) was able to use atmospheric H2S as sole sulphur source for growth. The foliarly absorbed H2S was rapidly metabolized into water-soluble, non-protein thiol compounds, including cysteine, and subsequently into other sulphur compounds in the shoots. In H2S-exposed plants, the accumulation of sulphur compounds in the shoots was nearly linear with the concentration (0.15–0.6 µl l–1) and duration of the exposure. Exposure of onion to H2S for up to 1 week did not affect the sulphur content of the roots. Secondary sulphur compounds formed a sink for the foliarly absorbed sulphide, and the sulphur accumulation upon H2S exposure could, for a great part, be ascribed to enhancement of the content of
-glutamyl peptides and/or alliins. Furthermore, there was a substantial increase in the sulphate content in the shoots upon H2S exposure. The accumulation of sulphate originated both from the pedosphere and from the oxidation of absorbed atmospheric sulphide, and/or from the degradation of accumulated secondary sulphur compounds. From studies on the interaction between atmospheric and pedospheric sulphur nutrition it was evident that H2S exposure did not result in a down-regulation of the sulphate uptake by the roots.
Key words:
Alliins, Allium cepa, -glutamyl peptides, hydrogen sulphide, onion, secondary sulphur compounds, sulphate, sulphur deficiency, sulphur deprivation, sulphur metabolism, thiols
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Introduction |
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TopAbstractIntroductionMaterials and methodsResults and discussionConclusionsReferences |
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Amongst other elements, sulphur is present in plant tissue in minor quantities only; its content varies strongly between species and ranges from 0.03–2 mmol g–1 dry weight (DW). Plants generally utilize the sulphate taken up by the roots as a sulphur source for growth and, prior to its assimilation, sulphate needs to be reduced to sulphide before it is metabolized into organic sulphur compounds. Plants contain a variety of sulphate transporters with specific functions in the uptake of sulphate by the roots, its transport to the shoot, and its subcellular distribution (Hawkesford and Smith, 1997
; Hawkesford, 2000, 2003; Hawkesford and Wray, 2000; Hawkesford et al., 2003). Roots contain all the enzymes necessary to reduce sulphate to sulphide, although the chloroplast appears to be the primary site for the reduction of sulphate to sulphide and its subsequent incorporation into cysteine (Brunold, 1990, 1993; Davidian et al., 2000). Cysteine is the sulphur donor for most other organic sulphur compounds in plants. The predominant proportion of the sulphur is present in proteins, as cysteine and methionine residues, where it is highly significant in the structure, conformation, and function (De Kok et al., 2002a). Sulphur is also required for the synthesis of various other compounds, such as thiols (glutathione), sulpholipids and secondary sulphur compounds (alliins, glucosinolates, phytochelatins), which play an important role in the physiology of plants, and in the protection and adaptation of plants against stress and pests. Sulphur deficiency will result in the loss of plant fitness, the plant's resistance to environmental stress and pests, and in decreased food quality and safety (De Kok et al., 2002a, c).
Under normal conditions, the rate of uptake and assimilation of sulphur will be in tune with the plant's sulphur need for growth, which can be defined as the rate of sulphur uptake and its assimilation considered necessary per gram plant biomass produced with time. When a plant is in the vegetative growth period, it can be calculated as follows (De Kok et al., 2000, 2002a):
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Despite their potential phytotoxic effects, plants are able to utilize atmospheric sulphur gases, namely, SO2, H2S, as the sulphur source for growth (Westerman et al., 2000a
, b; De Kok et al., 2002a, c; Tausz et al., 2003; Yang et al., 2003). The foliar uptake of these sulphur gases proceeds via the stomates and the rate of uptake is determined by both the stomatal conductance and the internal (mesophyll) resistance towards these gases (De Kok and Tausz, 2001; De Kok et al., 2002a, b). From calculating the plant's sulphur need and foliar uptake rate of sulphur gases, and subsequent laboratory experiments, it is evident that atmospheric levels of 
0.1 µl l–1 of these sulphur gases should be sufficient to cover the organic sulphur need for growth of most plant species, including onion (De Kok et al., 2000, 2002b; Table 1). Studies on the possible interaction between atmospheric and pedospheric sulphur nutrition have been shown to be helpful as a tool to get an insight into the regulation of sulphate uptake and sulphur assimilation, and the dissection of the signal-transduction pathways involved.
Allium species, namely, onion, garlic, leek, and chive, contain a variety of secondary sulphur compounds: -glutamyl peptides and alliins (S-alk(en)yl cysteine sulphoxides). The content of the secondary sulphur compounds is strongly dependent on the stage of development of the plant, temperature, water availability, and the level of nitrogen and sulphur nutrition (Randle et al., 1993, 1995; Randle, 2000; Randle and Lancaster, 2002; Coolong and Randle, 2003a, b). They form a potential sink for reduced sulphur, since, in onion bulbs, their content may account for up to 80% of the organic sulphur fraction (Schnug, 1993). Less is known about the content of secondary sulphur compounds in the seedling stage of the plant. It is assumed that alliins are predominantly synthesized in the leaves, from where they are subsequently transferred to the attached bulb scale (Lancaster et al., 1986). The biosynthetic pathways of synthesis of -glutamyl peptides and alliins are still ambiguous. -Glutamyl peptides are formed from cysteine (via -glutamyl cysteine or glutathione), and can be metabolized into the corresponding alliins via oxidation and subsequently hydrolysation by -glutamyl transpeptidases (Lancaster and Boland, 1990; Randle and Lancaster, 2002). However, other possible routes of the synthesis of -glutamyl peptides and alliins cannot be excluded (Granroth, 1970; Lancaster and Boland, 1990; Edwards et al., 1994; Randle and Lancaster, 2002). Alliins and -glutamyl peptides are known to have therapeutic qualities, and might have potential value as phytopharmaceutics (Haq and Ali, 2003). The alliins and their breakdown products (e.g. allicin) are the flavour precursors for the odour and taste of Allium species. Flavour is only released when plant cells are disrupted and the enzyme alliinase, from the vacuole, is able to degrade the alliins, yielding a wide variety of volatile and non-volatile sulphur-containing compounds (Lancaster and Collin, 1981; Block, 1992). The physiological function of -glutamyl peptides and alliins is rather unclear (Schnug, 1993). These compounds may have significance in chemical defence against insects and pathogens, and in the storage of nitrogen and sulphur (Lancaster and Boland, 1990). It has been suggested that, in onion bulbs, -glutamyl peptides may be the main storage form of nitrogen and sulphur, and they might be rapidly hydrolysed to alliins during sprouting and germination (Randle and Lancaster, 2002).
It remains to be investigated to what extent the accumulation of -glutamyl peptides and alliins is a consequence of an altered balance in the sulphur supply and in the actual sulphur requirement for structural growth during bulb formation. It is still unclear to what extent these compounds form a potential sink for excessive reduced sulphur during the earlier stages of development of Allium, for instance, in seedlings.
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Materials and methods |
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Seeds of onion (Allium cepa L. cv. Nerato F1; Nickerson-Zwaan, Made, The Netherlands) were germinated in vermiculite in a climate-controlled room. Two-week-old seedlings were transferred to 30 l tanks containing a 25% Hoagland nutrient solution, pH 5.9, and grown for 10 d for studies on the combined impact of sulphate nutrition and H2S exposure, and for 18 d in other experiments (Durenkamp and De Kok, 2002
). For studies on sulphate deprivation, MgCl2 replaced MgSO4 in the Hoagland nutrient solution and their chloride salts replaced all micronutrient sulphate salts.
For H2S exposure plants were transferred to stainless steel containers filled with a 25% Hoagland nutrient solution, pH 5.9, placed in 150 l cylindrical stainless steel cabinets with a polycarbonate top (Stuiver et al., 1992; Durenkamp and De Kok, 2002). Day and night temperatures were 20 °C and 16 °C, respectively, relative humidity was 40–50%, and the photoperiod was 14 h at a photon fluence rate of 300–350 µmol m–2 s–1 at plant height.
For determination of anions, total sulphur, and total nitrogen, shoot and roots were freeze-dried or oven-dried at 80 °C and subsequently pulverized by a Retsch microdismembrator (type MM2, Haan, Germany). There were no differences in the determinations of the metabolite content of freeze-dried and oven-dried samples (data not presented). Anions were extracted and determined as described before (Durenkamp and De Kok, 2002). Total sulphur in the tissues was reduced to sulphate by ashing and dissolving in strong acid and the turbidity of the samples was measured on a spectrophotometer at 450 nm after addition of BaCl2 (Durenkamp and De Kok, 2002). Total nitrogen in the tissues was reduced to ammonium by boiling in concentrated H2SO4 in the presence of a catalyser and ammonium was determined colorimetrically at 410 nm after reaction with Nessler's reagent (Durenkamp and De Kok, 2002). The organic sulphur and nitrogen content was calculated by subtracting the sulphate and nitrate content from the total sulphur and nitrogen content, respectively. Water-soluble, non-protein thiols and cysteine in shoot and roots were determined as described before (De Kok et al., 1988; Stuiver et al., 1992).
The relative growth rate (RGR) of plants was calculated using the ln-transformed plant fresh weight (FW) (Hunt, 1982).
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Results and discussion |
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Uptake of H2S by shoots of Allium and its impact on growth and thiol content
H2S is a phytotoxic gas and growth of susceptible species may already be negatively reduced upon prolonged exposure to atmospheric levels of 0.03 µl l–1 and higher (De Kok et al., 1998
, 2002b). The physiological basis for its phytotoxicity, and variation between species in susceptibility to H2S is still largely unclear. Sulphide is very reactive, and, similar to cyanide, it complexes with high affinity to metallo groups in proteins; this reaction is probably the primary biochemical basis for the phytotoxicity of H2S (De Kok et al., 1998, 2002b). It has been suggested that the degree of penetration of H2S into the meristems may be one of the most important factors determining its phytotoxicity. In general, dicotyledons are more susceptible to H2S than monocotyledons, since in the latter H2S has hardly any direct access to the vegetation point (De Kok et al., 2000; Stulen et al., 2000). Similarly, onion and other Allium species, as monocotyledons, appeared not to be susceptible to the potential phytotoxic effects of H2S (Durenkamp and De Kok, 2002, 2003). Plant biomass production was hardly affected by a 2-week exposure to relatively high atmospheric H2S levels from up to 0.3 µl l–1 (Durenkamp and De Kok, 2002), and even not upon exposure to 0.6 µl l–1 for 1 week (data not presented). The shoot:root ratio and dry matter content in shoot and roots were not affected upon H2S exposure (Durenkamp and De Kok, 2002, 2003).
Similar to observations with other species, the H2S uptake by shoots of onion followed saturation kinetics with respect to the H2S concentration and the saturation kinetics fitted in well with the Michaelis–Menten equation. The maximum H2S uptake rate (JH2Smax) was 1.1 µmol g–1 h–1 shoot FW and the H2S concentration at which half JH2Smax was reached (KH2S) was 1.5 µl l–1 H2S (Durenkamp and De Kok, 2002). It is evident that the uptake of H2S is largely determined by physiological factors, namely, the rate of assimilation of the deposited sulphide into cysteine by O-acetylserine (thiol)lyase and the subsequent incorporation into other organic sulphur metabolites.
The direct metabolism of atmospheric H2S generally results in an increased size and change in composition of the thiol pool in the shoot (De Kok et al., 1998, 2002b). In some species, after some delay, H2S exposure may also result in an enhanced thiol level in the roots, although to a lesser extent than that observed in shoots. The increase in size of the thiol pool is dependent on the H2S concentration, the level of sulphur nutrition, the exposure temperature, and plant age, and it varies strongly between species (De Kok et al., 1998, 2002b). The tripeptide glutathione is usually the most abundant thiol compound present in both shoot and roots. However, if the regulation of the uptake of sulphate by the roots is by-passed, and sulphur is directly supplied to foliar tissue, in either oxidized or reduced form, then not only the size, but also the composition, of the thiol pool changes, and, in addition to glutathione, high levels of cysteine and other thiols may occur (De Kok et al., 1998, 2002b, c).
A two-week exposure of the onion also resulted in an accumulation of thiols in the shoots at levels higher than 0.075 µl l–1 H2S (up to 3-fold at 0.3 µl l–1; Durenkamp and De Kok, 2002). Similar to previous observations, H2S exposure did not affect the thiol and cysteine content of the roots (Fig. 1). Short-term exposure measurements confirmed that, similar to observations with other species, the level of thiol accumulation in the shoots depended on the H2S concentration, already having reached a maximum level within 1 d of exposure, and having remained nearly constant during the 7-d exposure period (Fig. 1). The increase in thiol content was partially due to an increase in cysteine content (up to 25% of the thiols after 1 d at 0.6 µl l–1 H2S). O-acetylserine (thiol)lyase, the enzyme responsible for the fixation of atmospheric H2S into cysteine, is present in both chloroplasts and cytosol. The increase in size, and the altered composition of the thiol pool upon H2S exposure, could both be due to an enhanced synthesis of cysteine in the cytosol, beyond the existing systems of feedback control of sulphur reduction and assimilation in the chloroplast (De Kok et al., 2002b, c).
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H2S-induced increase in total sulphur and sulphate content in shoots of Allium
The onion formed a sink for atmospheric H2S and a 2-week exposure resulted in a substantial increase in the content of both total sulphur and sulphate in the shoots (3-fold at 0.3 µl l–1), whereas that in the roots remained unaffected (Durenkamp and De Kok, 2002
). A similar H2S-induced increase in the sulphur content was observed in shoots of a variety of A. cepa L. (onion) cultivars and other Allium species (A. fistulosum L. and A. porrum L.) upon prolonged exposure to 0.15 µl l–1 H2S (Durenkamp and De Kok, 2003). There was a nearly linear relation between the increase in total sulphur and sulphate content in the shoot and the H2S concentration (ranging from 0.075–0.3 µl l–1). There was a slight increase in total nitrogen content of the shoot, whereas that of nitrate and amino acids was hardly affected (Durenkamp and De Kok, 2002).
From short-term experiments, it was evident that the accumulation of total sulphur and sulphate upon H2S exposure occurred rapidly, and was already substantial after 2 d of exposure (Fig. 2). The total sulphur and sulphate content in the shoot increased nearly linearly with the H2S concentration, and the duration of the exposure was up to more than 3-fold at 0.6 µl l–1 H2S at a constant sulphate:total sulphur ratio of around 0.5. Short-term exposure did not affect the total sulphur and sulphate content in the roots (Fig. 2). The contents of total nitrogen and nitrate were 190 and 77 in the shoot, and 118 and 48 µmol g–1 FW in roots, respectively, and were not significantly affected upon H2S exposure (data not presented). In unexposed plants the organic molar N:S ratio was around 40 (Durenkamp and De Kok, 2002; Fig. 2), probably predominantly representing the molar ratio of N:S in the proteins (Dijkshoorn and Van Wijk, 1967). Upon H2S exposure the organic N:S ratio substantially decreased with the H2S concentration down to values around 10 upon prolonged exposure at the highest H2S levels. The latter may be ascribed to an increase in the content of non-protein organic sulphur compounds (Durenkamp and De Kok, 2002; Fig. 2). The molar N:S ratio in the secondary sulphur compounds is 
2 and, therefore, it is most probable that a great part of the increase in sulphur content upon H2S exposure is due to an enhancement of the content of alliins and/or its precursors (Durenkamp and De Kok, 2002, 2003).
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Interaction between atmospheric H2S and pedospheric sulphate nutrition in Allium
The origin of the accumulated sulphate in onion shoots upon H2S exposure was unclear. Onion shoots might transfer completely from pedospheric sulphate to atmospheric H2S as the sulphur source without a down-regulation of sulphate uptake by the root and transport to the shoot. On the other hand, the accumulated sulphate might originate from the oxidation of absorbed atmospheric sulphide and/or from the degradation of accumulated (secondary) sulphur compounds. In order to test the nature of sulphate accumulation in onion shoots upon H2S exposure, the impact of sulphate nutrition and H2S exposure on total sulphur and sulphate content was evaluated.
In general, the uptake of sulphate by the roots and its transport to the shoot appear to be the primary sites of regulation of sulphur assimilation, and are generally in tune with the plant's sulphur need for growth (Hawkesford and Wray, 2000; De Kok et al., 2002a). When onion seedlings were transferred from 0.5 mM sulphate (the sulphate level in a 25% Hoagland nutrient solution) to various levels of sulphate (up to 8 mM) for a week, it only slightly affected the sulphur content of shoot and roots (Fig. 3). There was a slight decrease in sulphate content at 1 mM sulphate in the nutrient solution. This might be explained by the fact that plants had been pre-cultivated at 0.5 mM for 2 weeks (Fig. 3) and were transferred to a higher sulphate level, which might have a de-repressing effect on the sulphate transporter(s). These data are in agreement with observations from other plant species that sulphate is taken up by the roots with high affinity and that the Vmax of sulphate uptake is generally already reached at pedospheric sulphate levels of 0.1 mM and lower, although it may be modulated by the level of sulphur nutrition (Hawkesford, 2000; Hawkesford and Wray, 2000; Hawkesford et al., 2003).
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When onion was grown under sulphate-deprived conditions for up to 7 d, it rapidly resulted in a decrease in the sulphate and total sulphur content in both shoot and roots (Fig. 4). If expressed on a plant basis, the amount of sulphur remained unchanged upon sulphate deprivation, while that of sulphate decreased, due to its assimilation into organic compounds and reflected by a decreasing sulphate:total sulphur ratio (Fig. 5). Upon sulphate deprivation, shoot growth started to decrease from day 4 onwards (data not presented) resulting in a decrease in the shoot:root ratio (Table 2). The latter is characteristic for sulphate-deprived plants (De Kok et al., 1997
, 2000, 2002c). However, after 7 d the relative growth rate of whole plants was not yet affected (Table 2). There were no visible symptoms of sulphur deficiency (e.g. leaf chlorosis), and other characteristics of the occurrence of severe sulphur deficiency, such as a strong increase in dry matter content (Table 2), and in the content of nitrate and free amino acids, were still absent (data not presented; De Kok et al., 1997, 2000, 2002c).
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When onion was sulphate-deprived and, simultaneously, exposed to 0.3 µl l–1 H2S, shoot growth was similar to that at sulphur-sufficient conditions (Table 2). The total sulphur content of the shoot increased substantially with the duration of the exposure both in sulphate-sufficient and sulphate-deprived plants. Similar to the preceding observations, the total sulphur content of the roots was not affected upon H2S exposure (Fig. 4). However, the total sulphur content of the sulphate-deprived roots decreased, although to a lesser extent than that of under sulphate-deprived conditions in the absence of H2S (Fig. 4). Similar to plants grown in sulphate-sufficient conditions, the increase in sulphur content in shoots of sulphate-deprived plants upon H2S exposure was partially due to an increase in sulphate content (Fig. 4). The total sulphur accumulation with time in sulphate-sufficient and sulphate-deprived plants upon H2S exposure was quite similar, which became evident when the total sulphur and sulphate content was expressed on a whole plant basis (Fig. 6).
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There was apparently no interaction between shoot and roots in sulphur nutrition at sulphate-sufficient conditions, since H2S exposure did not result in a down-regulation of uptake and metabolism of sulphate taken up by the roots. Still, there were considerable differences in the proportion of accumulated total sulphur in the organic sulphur fraction. Upon H2S exposure, less sulphur accumulated in the sulphate fraction in sulphate-deprived plants; the greater part was incorporated in the organic sulphur fraction as illustrated by a lower sulphate:total sulphur ratio (around 0.3; Fig. 5). The present data confirm that the absorbed atmospheric H2S can be metabolized and used as a sulphur source for plant growth. From the observations that in sulphate-deprived plants, H2S exposure also resulted in a net accumulation of sulphate (Fig. 5), it was evident that accumulated sulphate (also under sulphate-sufficient conditions) had to originate from the oxidation of absorbed atmospheric sulphide and/or from degradation of accumulated (secondary) sulphur compounds.
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Conclusions |
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TopAbstractIntroductionMaterials and methodsResults and discussionConclusionsReferences |
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From the present study, it is evident that shoots of onion (and other Allium species) form a potential sink for foliarly absorbed sulphur. It was already striking that, compared with most other plant species, onions had a relatively high capacity for H2S uptake (De Kok et al., 1998
, 2002b, c; Durenkamp and De Kok, 2002), even though this species had (under normal conditions) a rather low sulphur need for growth. When the regulation of the sulphate uptake by the roots was by-passed and plants were exposed to atmospheric H2S, it resulted in greatly increased sulphur contents in the shoots, whereas those of the roots remained unaltered. The accumulation of total sulphur in shoots of onion can, in part, be attributed to the metabolism of the absorbed H2S into secondary sulphur compounds, namely, -glutamyl peptides, alliins. The origin of the accumulated sulphate in onion upon H2S exposure needs to be investigated further. It is evident that it may originate from both the pedosphere and from oxidation of absorbed atmospheric sulphide, and/or from degradation of accumulated (secondary) sulphur compounds. In general, the synthesis of alliins is maximal during the formation of the bulbs. It is not yet clear to what extent all enzymes needed for the synthesis of alliins are functional during the seedling stage in the leaves of onion. Certain precursor compounds (-glutamyl peptides) might be formed in high amount upon H2S exposure and, subsequently, not further incorporated into alliins. The formed precursor compounds might be degraded and may, in part, be the cause of the observed sulphate accumulation.
The impact of H2S on sulphur metabolism in onion was quite different from that observed in other species. For instance in Brassica oleracea (curly kale), there was a direct interaction between the regulation of uptake of atmospheric H2S by the shoots and the uptake of sulphate by the roots (De Kok et al., 1997, 2000, 2002a, c; Westerman et al., 2000a, b). With an ample sulphate supply to the roots, the total sulphur content of this species was hardly affected by prolonged H2S exposure, not even at atmospheric levels higher than 0.2 µl l–1, which exceeded the sulphur requirement for growth by far. B. oleracea was able to transfer from sulphate to H2S as a sulphur source for its reduced sulphur, and the uptake and assimilation of atmospheric H2S by the shoot, and the uptake of sulphate by the roots were largely in tune, and adjusted to the actual sulphur need for growth. Upon H2S exposure, the sulphate uptake rate by the roots of B. oleracea was reduced to such extent that the proportion of sulphur absorbed from the atmosphere appears to be sufficient to cover the organic sulphur need for growth (De Kok et al., 2000, 2002a, b, c). Brassica species also contain secondary organic sulphur compounds, namely, glucosinolates (Schnug, 1990, 1993). In the vegetative parts of the plants, their content was generally low; it did not exceed 1–2% of the total sulphur content (Westerman et al., 2001). The content of the glucosinolates in the shoots was hardly affected by H2S exposure (Westerman et al., 2001).
Additional research on the identification of the accumulating sulphur compounds in Allium upon H2S exposure is currently being carried out. Further H2S impact studies may be helpful in the elucidation of the pathways of synthesis of -glutamyl peptides and alliins, and will give more insight into the possible physiological function of these secondary sulphur compounds.
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Acknowledgements |
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We would like to thank Dr Ineke Stulen for her contribution to the manuscript.
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References |
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