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Influence of Nitrogen and Sulfur Fertilization on theAlliin Content of Onions and GarlicElke Bloem a , Silvia Haneklaus a & Ewald Schnug aa Institute of Plant Nutrition and Soil Science, Federal Agricultural Research Centre(FAL), Bundesallee, Braunschweig, GermanyVersion of record first published: 23 Aug 2006.

To cite this article: Elke Bloem , Silvia Haneklaus & Ewald Schnug (2005): Influence of Nitrogen and Sulfur Fertilization onthe Alliin Content of Onions and Garlic, Journal of Plant Nutrition, 27:10, 1827-1839

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JOURNAL OF PLANT NUTRITION

Vol. 27, No. 10, pp. 1827–1839, 2004

Influence of Nitrogen and Sulfur Fertilization

on the Alliin Content of Onions and Garlic

Elke Bloem,* Silvia Haneklaus, and Ewald Schnug

Institute of Plant Nutrition and Soil Science, Federal Agricultural

Research Centre (FAL), Bundesallee, Braunschweig, Germany

ABSTRACT

Onion (Allium cepa L.) and garlic (Allium sativum L.) were among

the earliest cultivated crops and have been popular in folk medicine

for centuries. Alliins (cysteine sulfoxides) are the characteristic sulfur

(S) containing secondary metabolites of Allium species like onions,

shallot, garlic, leek and chives and they cause taste and sharpness and

are criteria for the pharmaceutical quality. The influence of the S

nutritional status on the content of secondary S containing

metabolites was shown for different crops such as oilseed rape,

mustard, nasturtium, and allium species. It was the aim of this study

to investigate the influence of the S and nitrogen (N) supply on the

alliin content of onion and garlic and to evaluate the significance for

crop quality. In a greenhouse experiment three levels of N and S were

*Correspondence: Elke Bloem, Institute of Plant Nutrition and Soil Science,

Federal Agricultural Research Centre (FAL), Bundesallee 50, D-38116,

Braunschweig, Germany; E-mail: elke.bloem@fal.de.

1827

DOI: 10.1081/LPLA-200026433 0190-4167 (Print); 1532-4087 (Online)

Copyright & 2004 by Marcel Dekker, Inc. www.dekker.com

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applied in factorial combinations of 0, 50, and 250mg pot�1 S and

250, 500, and 1000mgpot�1 N. 8 plants were grown in a Mitscherlich

pot containing 8 kg sand. Leaves and bulbs were sampled twice

during the growth period in order to follow up translocation

processes. The first sampling was carried out when leaves were

developed, but bulb growth had not yet started and the second one

during main bulb growth. An increasing S supply was related to an

increasing alliin content in leaves and bulbs of both crops, whereas

nitrogen fertilization had only a minor influence. The alliin content

in bulbs could be doubled by S fertilization. A translocation of alliin

from leaves to bulbs was found so that time of harvest has a strong

influence on the alliin content. At the beginning of plant develop-

ment high alliin contents were found in leaves, while with bulb

development they were translocated into this plant organ. The results

show that the potential health benefits of Allium species could be

distinctly improved by S fertilization.

Key Words: Allium species; Sulfur; Nitrogen; Phytopharmaceutical

quality; Nutritional quality.

INTRODUCTION

The chemical composition of Allium species is of interest inphytochemistry, plant–insect relationships, chemotaxonomy, flavorindustry, quality control of food and phytochemical preparations,pharmacognosy and medicine.[1,2] Allium species contain four S-alk(en)yl-L-cysteine sulfoxide; namely S-1-propenyl-, S-2-propenyl-,S-methyl- and S-propyl-L-cysteine sulfoxides,[3] which are S containingsecondary metabolites of phytopharmaceutical impact. S-1-propenyl-L-cysteine sulfoxide (iso-alliin) is the main form in onions while S-2-propenyl-L-cysteine sulfoxide (alliin) is the predominant form in garlic.[4]

The characteristic flavor of Allium species is caused after the enzymealliinase hydrolyses the cysteine sulfoxides to form pyruvate, ammoniaand S containing volatiles. In the intact cell alliin and related cysteinesulfoxides are located in the cytoplasm while the C–S lyase enzymealliinase is localized in the vacuole.[5] Disruption of the cell releases theenzyme, which causes subsequent �,�-elimination of the sulfoxides,ultimately affording volatile and odorous low molecular-weight organo-sulfur compounds.[6] The flavor and pungency is determined by decom-position products like propanethiol, propionaldehyde, di-1-propyldisulfide and methyl propenyl disulfide which have the purest andstrongest onion odor.[7] The cysteine sulfoxide content of Allium species is

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an important quality parameter with view to organoleptic features as itdetermines the taste and sharpness. The S fertilization has already beenshown to have a strong influence on the formation of S containingsecondary metabolites in vegetables and agricultural crops.[8–11] Onionflavor can be modified by cultivar and growth environment[12,13] and aprimary environmental factor which is influencing the flavor is as well theS supply, with higher available S generally resulting in greater flavorintensity[14–18] and changes in the composition of the different cysteinesulfoxides in onions.[19]

Additionally cysteine sulfoxides are of pharmaceutical value. Alliumspecies served as vegetables, condiments, and medical plants since ancienttimes. For example for garlic the oldest recorded literature with view toits use as medicine is dated at 2600–2100 B.C. when garlic was alreadywidely cultivated.[20] Onions are used as a household remedy for a longtime as it promote digestion, cure mild burns and asthma. Onions havealso a therapeutic effect on vascular diseases such as thrombosis,arteriosclerosis, hyperlipidemia and rheumatic arthritis because thehuman platelet aggregation is strongly inhibited in vitro by componentswhich are derived from the lachrymatory factor (thiopropanal S-oxide)which is build by the degradation of iso-alliin.[4] Garlic is used againstarteriosclerosis, high blood pressure, and has been shown to haveantibacterial, antifungal, antiviral and antiprotozoal activities. It alsomodulates the cardiovascular and immune system and has antioxidativeand anticancerogenic properties.[20] Therefore the cysteine sulfoxidecontent of Allium species is an important quality parameter.

The main problem in realizing high and constant levels of alliin istheir instability: the decomposition of iso-alliin in Allium cepa starts in themoment when the plant material is damaged and 93% are decomposedby alliinase within 2–3min.[21] Therefore harvesting technique, processingand freshness of the product are of great importance to minimize losses ofthe active compound.

Allium crops are of great economic importance as onions areconsumed mostly after tomatoes and cabbages from cultivated vegetablecrops with a worldwide production of 50� 1012 t in 2002 and also garlicwas produced extensive with 12� 1012 t.[22]

The quality of vegetables rather than to increase yields has been ofincreasing interest, because customers are interested more and more inthe nutritional value of food. This led to the development of so-called‘‘functional food’’. Despite the limited knowledge of European con-sumers on the concept, functional foods represent one of the fastestgrowing markets in the developed world, representing 32 billion US$ andan annual growth of 15 to 20% worldwide.[23] Functional foods are

N and S Fertilization on the Alliin Content of Onions and Garlic 1829

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similar in appearance to conventional foods and are consumed as part ofthe diet. However, in addition to their nutritional function, they aredesigned to offer a particular health benefit over and above thetraditional nutrients they contain. The problem is that there is nocommon legal definition for functional food and it is somewhat betweenfood and drugs. Today the possible risk from enriched foodstuff cannotbe estimated because it was never investigated before what are the risksfrom very high doses of nutrients or secondary metabolites, if there arecompetitive interactions of nutrients and additionally the physiologicalaction of many plant substances is not fully understood. This could beseen just recently when dangerous side effects of Kava kava (Pipermethysticum) were discovered, which may lead to liver failure in the worstcase. Kava was a herbal supplement that was used as tension relaxer andalternative for valium and it was sold on a large scale.[24]

It is much more recommendable to eat a balanced diet fromnatural high quality foodstuff where the ingredients are balanced in thenatural way.

It was the aim of this study to investigate the influence of S and Nnutrition on the alliin content of onion and garlic, and to assess thepossibilities to produce Allium crops of high nutritional quality withrespect to health promoting ingredients.

MATERIALS AND METHODS

Experimental Design

A bifactorial greenhouse experiment was conducted with 3 S levels (0,50, and 250mg S per pot as K2SO4) and 3 N levels (250, 500, and 1000mgN per pot as NH4NO3). Sulfur was fertilized before planting andpotassium was balanced with KCl. The fertilization with N, Ca, and Pwas split into two equal doses from which the first was given beforeplanting and the second 2 weeks (onions) or 4 weeks (garlic) later. Allother nutrients (Mg, Mn, Zn, Cu, Mo, Fe, B) were applied in aphysiological optimum rate before planting. In each Mitscherlich-potcontaining 8 kg of sand, 8 onions of the variety ‘Stuttgarter Riese’ or 8garlic bulbs of the variety ‘Thermidrome’, respectively were grown. Eachtreatment had four replicates. The first sampling was carried out 4(onions) or 7 weeks (garlic) after planting, when leaves were developed,but bulb growth had not yet started and the second one 5 (onions) or7 weeks (garlic) later at main growth of the bulbs. Leaves and bulbswere sampled separately and the samples were immediately shock-frozen

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in liquid nitrogen and subsequently freeze-dried to prevent the decom-position of the alliins.

Chemical Analysis

Total N was determined employing the Kjeldahl method. Theextraction of total S was performed by microwave digestion with HNO3/H2O2 (4 : 1) and final determination by ICP-OES. The iso-alliin contentof leaves and bulbs was determined by HPLC.[9]

Statistical Analysis

For statistical analysis the ANOVA procedure of the CoHortsoftware package was used to segregate different sources of variation.[25]

RESULTS AND DISCUSSION

Fertilization with N and S was effective as both, the total N and totalS content in the plant material were significantly increased (Tables 1and 2). Nitrogen fertilization increased the N content in leaves on anaverage from 34.7 to 48.1mg g�1 N and the S content was increased byS fertilization on an average from 2.3 to 5.9mg g�1 S at the first samplingdate (Table 1). The N and S content was strongly correlated with theN and S fertilization, respectively (Table 2). There were also interactionsbetween N and S: the total S content of onion leaves was highlycorrelated with the N fertilization in that way that the S content of leavesdecreased with increasing N fertilization and the total N content of onionbulbs decreased with increasing S fertilization (Table 2). The sameobservations were made by Freeman and Mossadeghi[15] for garlic plantswhere the N content decreased from 4.05 to 2.93% with S fertilizationand by Randle,[19] who found decreasing total bulb S contents in responseto increasing N fertilization. Extreme N : S ratios of up to 100 : 1 weredetermined in the bulbs of onions at the second sampling date when no Sand the full dose of N were applied. N : S ratios of 5 : 1 to 10 : 1 in thebulbs at the second sampling reflected a good N and S nutrition of onionsand garlic. Excess N has further disadvantages as foliar growth isstimulated and bulb growth depressed, the firmness of the bulb isdecreasing and the post harvest shelf life is affected.[26,27]

N and S Fertilization on the Alliin Content of Onions and Garlic 1831

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Table

1.

Totalnitrogen,sulfur,andalliincontents

inleaves

andbulbsofA.cepaandA.sativum

atdifferentgrowth

stages.

N-supply

(mgpot�

1)

S-supply

(mgpot�

1)

TotalN

TotalS

Alliin

TotalN

TotalS

Alliin

(mgg�1)

(mgg�1)

(mgg�1)

(mgg�1)

(mgg�1)

(mgg�1)

Leaves

Bulbs

1st

2nd

1st

2nd

1st

2nd

1st

2nd

1st

2nd

1st

2nd

OnionSamplinga

250

031.7

22.2

2.4

1.3

1.3

0.2

13.0

7.8

1.7

0.4

0.7

0.6

250

50

35.8

21.8

4.8

2.5

6.6

4.2

16.1

7.6

2.7

1.4

0.4

2.1

250

250

36.7

20.8

6.7

3.4

10.3

6.4

17.5

6.7

4.0

1.8

0.4

2.6

500

039.0

30.5

2.2

1.4

6.0

3.6

23.1

17.9

1.7

0.2

0.5

1.8

500

50

40.8

23.2

4.4

2.0

6.3

2.0

19.8

12.4

3.0

1.0

1.9

1.4

500

250

41.8

23.1

6.1

3.1

9.3

5.6

21.8

12.9

3.6

2.4

0.3

3.5

1000

047.1

30.1

2.3

1.3

8.0

0.2

35.9

22.3

1.9

0.3

0.5

0.9

1000

50

47.6

30.5

4.5

1.8

5.6

0.8

30.2

19.1

2.7

1.0

1.3

1.3

1000

250

49.7

25.1

5.0

2.8

7.8

4.1

33.1

17.4

3.7

2.3

1.7

3.4

Garlic

Samplinga

250

038.8

27.0

5.0

3.2

13.1

5.9

26.5

14.1

2.9

0.9

3.0

1.1

250

50

36.5

25.3

6.7

5.5

16.4

11.4

26.0

11.6

5.2

1.9

4.7

3.4

250

250

38.6

24.6

8.2

6.6

15.8

15.6

24.9

13.7

4.9

2.5

4.0

2.1

500

041.0

36.5

4.8

2.9

9.3

4.4

23.4

20.9

2.7

0.6

5.1

0.5

500

50

39.9

34.1

6.8

4.9

16.1

9.8

29.6

20.0

5.1

2.2

8.4

3.2

500

250

38.6

30.2

8.4

7.6

19.8

18.7

28.0

16.0

7.0

3.7

6.4

3.6

1000

043.5

38.8

6.0

4.1

16.1

5.5

33.4

23.0

4.2

1.1

4.4

0.9

1000

50

45.9

35.1

6.5

5.8

15.5

12.0

32.5

22.6

4.1

2.6

3.7

2.7

1000

250

46.2

36.2

7.1

6.7

15.1

2.7

35.0

21.3

5.4

3.3

9.1

3.1

a1st

sampling4(onions)

and7weeks(garlic)after

planting;2ndsampling9(onions)

and14weeks(garlic)after

planting.

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Influence of Nitrogen and Sulfur Fertilization on the

Alliin Content of Onion and Garlic

Sulfur fertilization significantly increased the alliin content in leaves

and bulbs of Allium cepa and Allium sativum. In both Allium species the

alliin content increased by about 4mg g�1 in leaves (1st and 2nd

sampling) and 2mg g�1 in bulbs (Fig. 1). For A. cepa and A. sativum a

close relationship was found between S fertilization and alliin content in

leaves at both sampling dates and in bulbs at the second sampling. At the

first sampling the leaves were in the main growth while bulb growth had

not jet started. Therefore, at this time, the bulbs did not function as

storage organs but as nutrient sources for the vegetative plant growth.

Thus the nutrient and alliin concentration in the bulbs at the first

sampling are not dependent on the nutritional status.In general no significant influence of the N fertilization on the alliin

content was found but there was a tendency that a higher N supply

resulted in a decreased alliin content. A negative relationship was found

between the N content of onions and garlic and the alliin content in older

leaves (2nd sampling) (Fig. 2). Changes in the synthesis of flavor

precursors in onions were also observed: an increasing N supply led to an

Table 2. Summary of ANOVA (F-test) for the different sources of variance.

Source of variation

Alliin Total S Total N

Leaf Bulb Leaf Bulb Leaf Bulb

S fertilization (S) Onion *** *** *** *** ns **

Garlic *** * *** *** * ns

N fertilization (N) Onion ns ns *** ns *** ***

Garlic ns ns ns ns *** ***

S�N Onion *** * * ns ns *

Garlic *** ns ** ns * ***

Time of harvest (T) Onion *** *** *** *** *** ***

Garlic *** *** *** *** *** ns

T� S Onion ns *** *** ns *** ns

Garlic ns ns ns ns * ns

T�N Onion ** ns ns ns ** ***

Garlic * ns ns ns *** ns

T� S�N Onion * *** ns ns ns ns

Garlic * ns ns ns ns ns

ns: non-significant; and significant at *P< 0.05, **P< 0.01, and ***P< 0.001.

N and S Fertilization on the Alliin Content of Onions and Garlic 1833

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increased activity of the S-methyl-1-cysteine sulfoxide pathway in favorof the iso-alliin synthesis.[26,28]

The correlation matrix (Fig. 2) reveals that the alliin content of onionand garlic leaves was strongly correlated with the S status of the crop atthe first sampling date. The alliin content of different plant parts wereintercorrelated which is due to translocation processes from leaves tobulbs.

Translocation of Alliin in Onion and Garlic

During plant growth alliin is translocated from leaves to bulbs whatis reflected by higher alliin contents in leaves at the first sampling date(Table 1, Fig. 1). Cysteine sulfoxides are synthesized in the leaves andtranslocated immediately into the bulbs.[29] Therefore, the alliin contentincreases in bulbs during plant development what was observed foronions (Fig. 1). The alliin content in garlic bulbs decreased from the firstto the second sampling most likely due to a dilution effect because of thefast bulb growth at this stage of plant growth. At the beginning of plantdevelopment high alliin concentrations of up to 10.3mg g�1 in onionsand up to 19.8mg g�1 in garlic were found in the leaves while theconcentrations in the bulbs were significant lower with values between 0.3and 1.9mg g�1 in onions and 3.0 to 9.1mg g�1 in garlic (Table 1). At thesecond sampling the alliin content of the leaves was distinctly lower and

Figure 1. Influence of sulphur fertilization on the alliin content in leaves and

bulbs of onion and garlic at two different growth stages (1st sampling: vegetative

growth, 2nd sampling: main bulb growth)

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the content in the bulbs started to increase in onions what indicate that atranslocation of iso-alliin into the bulbs took place.

The proportion of total S which was bound in alliin was as high as74% in bulbs of onions at the 2nd sampling when no S and the full doseof N was applied while the proportion in the leaves was only between 0.4and 2.6%. This indicates that at this growth stage the bulbs did alreadyact as storage organ for secondary metabolites while in the leavesdifferent metabolic processes compete for S and the builded alliin istranslocated into the bulbs nearly completely when S is a limiting factor.Compared to S only a low amount of N is bound in alliin. On an average21% of S, but only 0.9% of N are bound as iso-alliin in onion.

Figure 2. Correlation matrix for the sulfur, nitrogen, and alliin content in leaves

and bulbs of onion (Allium cepa) and garlic (Allium sativum) at different growth

stages (numbers indicate the sampling date: 1: vegetative growth, 2: main bulb

growth)

N and S Fertilization on the Alliin Content of Onions and Garlic 1835

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Enhancement of Product Quality by Fertilization

The strong influence of the S nutritional status on the alliin content ofAllium species emphasizes the possibilities to enhance the nutritional andphytopharmaceutical value of the crops by an adequate S supply. Thereare innumerable health products made from garlic on the market and it isconspicuous that on most products only the amount of garlic is mentionedfrom which the oil is derived and not the concentrations of activecompound. The reason is most likely the high variability of the alliinconcentration in dependence on the variety, environmental conditions,harvest conditions and storage. A controlled S supply could be apossibility to produce garlic of a more constant product quality.

A simple theoretical calculation can show, howmuch the profit can beenhanced by S fertilization. If the assumption is made that the price of aphytopharmaceutical product from garlic is only determined by thecontent of the active compound alliin, than the price per gram alliin wouldbe in the range of 45–50E (estimated exemplary from the selling price of agarlic product). An average yield for garlic is 60–100 dt/ha[30] whatcorrespond with about 6000–10,000 kg of dry matter. An enhancement ofonly 1mg alliin per gram dry matter would increase the alliin content ofthe end product by 6–10 kg what correspond to 270,000–500,000E. Thereality is that the price of a product is only determined to a low part by theconstituents, but also if the alliin content determines only 1% of the pricethe possible increase in value by fertilization is significant with 2700–5000E and additionally the product quality with respect to the alliincontent is more stable with S fertilization.

The possibility to enhance the concentration of active compounds isnot only important for the phytopharmaceutical industry but also for thepossibility to produce high quality foodstuff. The world health organi-zation (WHO) is warning against health in form of pills, which containisolated active compounds because the action of medical plants is basedon several ingredients[31] and in most cases the combination of differentingredients is not fully understood. Natural plants are like ‘‘a cocktail ofactive compounds’’ and the action of one isolated active compound canbe negligible in the worst case. Therefore, it is recommendable to take innatural food that is produced in such a way that a maximum of healthyingredients is guaranteed.

CONCLUSIONS

Generally, a close relationship between S supply and alliin contentwas found for onion and garlic. In comparison, the alliin and N content

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either showed no relation or was correlated inversely. The results revealthat the S supply was an important parameter for the nutritional qualityof onion and garlic and that the S fertilization was an important tool toincrease the nutritional and phytopharmaceutical quality. Field trialshave shown that the daily intake of only one onion which was fertilizedwith S would be sufficient to cover a demand of 12mg (iso)alliin whichcorresponds to the recommended daily intake of alliin.[32] In contrast, itwould be necessary to eat two bulbs from fresh onions grown at a low Ssupply for a similar dose.[33]

With respect to phytopharmaceutical products from garlic claimsshould be entered that the concentration of at least one active compoundlike the alliin as a leading substance should be declared to give theconsumer the chance to compare products by their phytopharmaceuticalvalue and to choose high quality products.

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2. Velısek, J.; de Vos, R.H.; Schouten, A. HPLC determination of alliinand its transformation products in garlic and garlic-containingphytomedical preparations. Potrav. Vedy 1993, 11 (6), 445–453.

3. Block, E. The organosulfur chemistry of the genus Allium:Implications for organic sulfur chemistry. International Ed.(England). Angewandte Chemie 1992, 31, 1135–1178.

4. Kawakishi, S.; Morimitsu, Y. Sulfur Chemistry of onions andinhibitory factors of the arachidonic-acid cascade. ACS SYM. SER.1994, 546, 120–127.

5. Lancaster, J.E.; Collin, H.A. Presence of alliinase in isolated vacuolesand alkyl cysteine sulphoxides in the cytoplasm of bulbs in onion(Allium cepa). Plant Sci. Lett. 1981, 22, 169–176.

6. Block, E.; Calvey, E.M. Facts and Artifacts in Allium Chemistry.ACS SYM. SER. 1994, 564, 63–79.

7. Bakr, A.A.; Gawish, R.A. Current studies on onion and its pungencyPart 2. Interactive effects of sulfur fertilization and drying under theaspect of solar energy utilization. Nahrung 1998, 42 (2), 94–101.

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