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Variation and Distribution of Glucosinolates in 42 Cultivars of Brassica oleracea Vegetable Crops

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Brassica vegetables are known to contain glucosinolates that are precursors for bioactive compounds like isothiocyanates that have been shown to play an important role in human health. This study reports the results of a screening of 11 Brassica oleracea crops consisting of 42 cultivars (6 white cabbage, 5 red cabbage, 7 Brussels sprouts, 2 kale, 1 tronchuda, 3 oxheart cabbage, 2 kohlrabi, 6 broccoli, 5 cauliflower, 3 romanesco and 2 Savoy cabbage). All these cultivars were cultivated under the same conditions on a single location in the same season. The variation found in the level of glucosinolates is expected to be mainly due to the genetic variation. A large variation was observed in the level and profile of glucosinolates. Total glucosinolates varied from 14 to 625 μmol/100 g fresh weight. Glucoraphanin, the precursor of the isothiocyanate sulforophane, varied from 0 to 141 μmol/100 g fresh weight. Within broccoli glucoraphanin varied from 27 to 141 μmol/100 g fresh weight. Glucoiberin that is structurally related to glucoraphanin varied from 6 to 397 μmol/100 g fresh weight. Within broccoli glucoiberin varied from 21 to 397 μmol/100 g fresh weight
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Variation and Distribution of Glucosinolates in 42 Cultivars of Brassica
oleracea Vegetable Crops
R. Verkerk, S. Tebbenhoff and M. Dekker
Product Design and Quality Management Group
Department of Agrotechnology and Food Sciences
Wageningen University
Wageningen
The Netherlands
Keywords: cabbage, broccoli, Brussels sprouts, cauliflower, kale, Romanesco, kohlrabi,
genetic variation, glucoraphanin
Abstract
Brassica vegetables are known to contain glucosinolates that are precursors
for bioactive compounds like isothiocyanates that have been shown to play an
important role in human health. This study reports the results of a screening of 11
Brassica oleracea crops consisting of 42 cultivars (6 white cabbage, 5 red cabbage, 7
Brussels sprouts, 2 kale, 1 tronchuda, 3 oxheart cabbage, 2 kohlrabi, 6 broccoli, 5
cauliflower, 3 romanesco and 2 Savoy cabbage). All these cultivars were cultivated
under the same conditions on a single location in the same season. The variation
found in the level of glucosinolates is expected to be mainly due to the genetic
variation. A large variation was observed in the level and profile of glucosinolates.
Total glucosinolates varied from 14 to 625 µmol/100 g fresh weight. Glucoraphanin,
the precursor of the isothiocyanate sulforophane, varied from 0 to 141 µmol/100 g
fresh weight. Within broccoli glucoraphanin varied from 27 to 141 µmol/100 g fresh
weight. Glucoiberin that is structurally related to glucoraphanin varied from 6 to
397 µmol/100 g fresh weight. Within broccoli glucoiberin varied from 21 to
397 µmol/100 g fresh weight.
INTRODUCTION
Fruits and vegetables are abundant sources of various, extensively studied, health-
protective phytochemicals. One important group of these phytochemicals is that of the
glucosinolates. Glucosinolates (GS) comprise a group of thioglucosides naturally
occurring in Brassica vegetables such as broccoli, cauliflower, radish, Brussels sprouts
and cabbage. Glucosinolates co-exist with, but are physically separated from the
hydrolytic enzyme myrosinase in the intact Brassica plant. Upon mechanical injury of the
tissue, the enzyme and substrate come into contact resulting in hydrolysis (Mithen et al.,
2000). The products of GS hydrolysis, particularly the isothiocyanates and indoles, have
been shown to act as anticarcinogens by inhibition of phase I enzymes responsible for
bioactivation of carcinogens and by induction of phase II detoxification enzymes that
affect xenobiotic transformations (Talalay and Fahey, 2001). Research is ongoing to
establish the biological activities of dietary glucosinolates and breakdown products, their
bioavailability and metabolism (Mithen et al., 2000).
Epidemiological studies indicate that a diet rich in Brassica vegetables can reduce
the risk from a number of cancers (Van Poppel et al., 1999; Verhoeven et al., 1997).
However, up to now epidemiology cannot reproducibly correlate protection against
certain cancers or other diseases with specific vegetables, subgroups or individual
components. A plausible explanation for this can be the lack of realistic intake data of
specific health protective phytochemicals. Assessment of accurate dietary intake of
phytochemicals thus can play a crucial role. With more knowledge on the effects of the
complete vegetable production chain a more effective choice can be made on how to
enhance phytochemical levels in the final consumed product. Moreover, epidemiological
studies can possibly be improved by correcting phytochemical intake data for different
steps in the food production chain. Previously we have demonstrated a large variability in
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Proc. IS on Vegetable Safety and Human Health
Eds.: Hongju He and Wei Liu
Acta Hort. 856, ISHS 2010
levels of glucosinolates within a food production chain of Brassica vegetables (Dekker et
al., 2000; Dekker and Verkerk, 2003, 2005).
In this article we present a comparative study of glucosinolate distribution and
variability between and within groups of the most widely consumed Brassica vegetables
such as different types of cabbage, broccoli, cauliflower, kale and Brussels sprouts.
MATERIAL AND METHODS
Materials
The various Brassica vegetables were commercial hybrids supplied by Bejo Zaden
BV (Warmenhuizen, The Netherlands). The plants were grown on the same field (2002)
under standard cultivation and harvest conditions. At optimum maturity five plants were
harvested of each cultivar. All the edible parts of the vegetables were used for
glucosinolate analysis. The vegetables were chopped, mixed thoroughly and directly
frozen with liquid nitrogen. The frozen material was ground in a Waring Blender (Model
34BL99, Dynamics Corp. of America, New Hartford, Connecticut, USA) and stored at
-30°C until further analysis.
Glucosinolate Analysis
Individual glucosinolates were analysed using high performance liquid
chromatography (HPLC) following on-column desulphation as described by Verkerk et al.
(2001). Values are reported as µmol/100 g fresh weight (FW).
RESULTS AND DISCUSSION
The results of the analysis of the individual glucosinolate levels of the 42 cultivars
of the 11 Brassica oleracea crops are given in Table 1.
Broccoli
The predominant glucosinolate in broccoli is glucoraphanin, ranging from 26.6 to
141.2 µmol/100 g FW, with the exception of cultivar ‘Bordeaux’ (purple sprouting
broccoli) that has an exceptionally high level of glucoiberin (396.5 µmol/100 g FW). The
other broccoli varieties had glucoiberin levels ranging from 20.6 to 52.2 µmol/100 g FW.
No sinigrin was detected in broccoli, with the exception of ‘Bordeaux’.
Brussels Sprouts
The total level of glucosinolates in Brussels sprouts is, on average, the highest of
all the tested Brassica vegetables. The predominant glucosinolate in Brussels sprouts is
sinigrin, ranging from 51.9 to 310.9 µmol/100 g FW, followed by progoitrin, ranging
from 25.3 to 157.2 µmol/100 g FW.
Cauliflower
Cauliflower contains relatively low amounts of glucosinolates. Glucoiberin is the
predominant glucosinolate ranging from 7.6 to 34.2 µmol/100 g FW.
Kale In one of the varieties glucoiberin is the predominant glucosinolate, while in the
other one more gluconasturtiin is present.
Kohlrabi
Kohlrabi contains relatively low amounts of glucosinolates. The red variety
(‘Kolibri’) contains four times more compared to the white variety (‘Korist’).
Oxheart Cabbage
The total glucosinolate level of oxheart cabbage ranges from 85 to 165 µmol/
100 g FW. In two of the three varieties glucoiberin has the highest levels, ranging from
64
31.2 to 72.0 µmol/100 g FW. The other variety (‘Bejo 2574’) has a high level of
glucobrassicin (90.7 µmol/100 g FW).
Red Cabbage
Red cabbage has relatively high levels of glucoraphanin, ranging from 19.8 to
105.3 µmol/100 g FW, which is in the same range as the tested broccoli varieties. Other
glucosinolates with relatively high levels are glucoiberin, progoitrin, sinigrin and
gluconapin. The total level of glucosinolates ranges from 140 to 381 µmol/100 g FW.
Romanesco
Romanesco contains relatively low amounts of glucosinolates, ranging from 46 to
53 µmol/100 g FW.
Savoy Cabbage
Savoy cabbage contains predominantly glucoiberin and sinigrin. The ‘Wirosa’
variety has an exceptional high level of glucoiberin (289.8 µmol/100 g FW) and total
glucosinolates (482 µmol/100 g FW).
White Cabbage
Sinigrin and glucoiberin are the glucosinolates with the highest levels in white
cabbage. The total level ranges from 127 to 241 µmol/100 g FW.
Tronchuda
Only one variety of tronchuda (Portuguese kale) was tested. It contains relatively
low amount of glucosinolates. The predominant glucosinolate was glucoiberin
(22.1 µmol/100 g FW).
CONCLUSIONS
A large variation was observed in the level and profile of glucosinolates of 11
Brassica oleracea crops consisting of 42 cultivars (6 white cabbage, 5 red cabbage, 7
Brussels sprouts, 2 kale, 1 tronchuda, 3 oxheart cabbage, 2 kohlrabi, 6 broccoli, 5
cauliflower, 3 romanesco and 2 Savoy cabbage). Total glucosinolates varied from 14 to
625 µmol/100 g fresh weight. Glucoraphanin, the precursor of the isothiocyanate
sulforophane, varied from 0 to 141 µmol/100 g fresh weight. Within broccoli
glucoraphanin varied from 27 to 141 µmol/100 g fresh weight. Glucoiberin that is
structurally related to glucoraphanin varied from 6 to 397 µmol/100 g fresh weight.
Within broccoli glucoiberin varied from 21 to 397 µmol/100 g fresh weight.
Since all cultivars were cultivated under the same conditions on a single location
in the same season, the observed variation in the level of glucosinolates is expected to be
mainly due to the genetic variation. Even within the same vegetable type the variation can
be very large.
By selection of cultivars the level of desirable glucosinolate can be enhanced
considerably, which can lead to a substantial increase of the intake of health promoting
glucosinolates even without increasing the overall vegetable consumption. To reach this
goal also the critical points in the food supply chain that determine the retention of
glucosinolates in the finally consumed product (industrial processing and consumer
preparation) have to be optimized and controlled.
Literature Cited
Dekker, M., Verkerk, R. and Jongen, W.M.F. 2000. Predictive modelling of health aspects
in the food production chain, a case study on glucosinolates in cabbage. Trends in
Food Science & Technology 11(4/5):174-181.
Dekker, M. and Verkerk, R. 2003. Dealing with Variability in Food Production Chains: A
Tool to Enhance the Sensitivity of Epidemiological Studies on Phytochemicals. Eur. J.
Nutri. 42:67-72.
65
66
Dekker, M. and Verkerk, R. 2005. Modelling the Consequences of Variability in Food
Production Chains on Human Health. Acta Hort. 674:71-76.
Mithen, R.F., Dekker, M., Verkerk, R., Rabot, S. and Johnson, I.T. 2000. The nutritional
significance, biosynthesis and bioavailability of glucosinolates in human foods. J. Sci.
Food Agric. 80:967-984.
Talalay, P. and Fahey, J.W. 2001. Phytochemicals from cruciferous plants protect against
cancer by modulating carcinogen metabolism. Journal of Nutrition 131(11
supplement):3027S-3033S.
Van Poppel, G., Verhoeven, D.T.H., Verhagen, H., Goldbohm, R.A. et al. 1999. Brassica
vegetables and cancer prevention. Epidemiology and mechanisms. Advances in
Experimental Medicine and Biology 472:159-68.
Verhoeven, D.T.H., Verhagen, H., Goldbohm, R.A., van den Brandt, P.A. and van Poppel,
G.A. 1997. A review of mechanisms underlying anticarcinogenicity by brassica
vegetables. Chem. Biol. Interact. 103:79-129.
Tables
Table 1. Glucosinolate levels (µmol/100 g fresh weight) of Brassica oleracea varieties.
variety
glucoiberin
progoitrin
sinigrine
raphanin
napoleiferin
glucoalysin
gluconapin
4OH-glucobrassicin
glucobrassicanapin
glucobrassicin
gluconasturtiin
4-methoxyglucobrassicin
neoglucobrassicin
total
BROCCOLI
Alborada 25.9 5.0 69.2 3.9 13.7 8.4 7.5 134
Belstar 26.2 7.4 130.1 1.5 3.6 29.6 9.0 6.8 214
Bordeaux 396.5 5.9 15.7 26.6 42.1 2.7 24.2 10.5 9.6 534
Coronado 52.2 9.0 141.2 0.9 3.4 1.5 23.6 12.7 20.1 265
Lucky 20.6 5.5 35.7 1.2 6.1 6.9 5.1 4.4 86
Surveyor 26.0 5.0 57.4 1.1 2.3 14.4 6.3 8.6 121
BRUSSELS' SPROUTS
Dominator 83.3 93.2 310.9 9.2 47.6 3.3 54.8 11.0 11.7 625
Doric 38.2 157.2 149.8 26.4 0.4 2.1 110.8 3.1 4.5 60.5 9.9 5.1 0.7 569
Franklin 51.1 105.6 141.5 27.9 1.1 72.9 0.7 101.7 12.2 2.5 517
Glenroy 37.0 48.3 122.5 11.7 22.1 3.3 0.6 76.7 1.9 7.6 332
Maximus 91.5 25.3 64.5 22.8 36.6 2.0 2.5 28.3 9.2 3.4 0.4 287
Nautic 37.0 67.1 51.9 41.8 24.3 32.0 0.8 10.6 43.9 9.2 2.3 1.1 322
Revenge 47.5 111.8 202.3 8.5 52.2 2.6 37.9 7.3 8.7 479
CAULIFLOWER
Cassius 7.6 3.6 4.9 0.7 1.6 3.5 0.5 1.4 4.9 2.0 0.7 31
Encanto 10.5 6.1 7.4 3.6 9.4 0.3 0.7 2.5 1.2 42
Jerez 16.8 4.8 12.4 2.8 2.7 2.7 2.3 1.4 46
Panther (green) 34.2 3.4 7.9 2.1 4.3 0.8 4.8 1.7 59
Skywalker 10.2 6.1 6.2 3.5 2.1 0.3 3.3 0.8 33
67
67
68
Table 1. Continued.
variety
glucoiberin
progoitrin
sinigrine
raphanin
napoleiferin
glucoalysin
gluconapin
4OH-glucobrassicin
glucobrassicanapin
glucobrassicin
gluconasturtiin
4-methoxyglucobrassicin
neoglucobrassicin
total
KALE
Redbor 23.4 6.1 10.4 6.6 3.6 6.7 2.8 68.0 4.9 27.2 160
Riphor 35.0 6.3 20.0 1.7 9.4 4.9 5.2 3.5 14.0 100
KOHLRABI
Kolibri 12.8 28.6 0.8 4.8 1.0 3.1 1.1 52
Korist 6.4 1.0 3.3 1.7 12
OXHEART CABBAGE
Bejo 2574 32.3 1.6 20.0 2.1 1.7 2.6 0.5 90.7 2.6 8.7 1.5 164
Bejo 2575 72.0 6.3 45.1 9.2 1.1 8.3 19.2 4.1 165
Capricorn 31.2 5.9 24.6 5.0 9.1 6.1 3.0 85
RED CABBAGE
Azurro 19.5 30.5 31.4 19.8 0.8 25.7 0.7 10.2 1.9 140
Buscaro 51.6 75.7 79.5 66.2 0.4 0.4 59.3 1.6 6.0 2.8 344
Huzaro 21.9 37.3 25.5 105.3 0.8 1.4 26.0 2.2 9.9 3.5 234
Integro 30.1 42.3 53.1 61.0 0.4 35.2 1.6 9.5 1.2 234
Pesaro 57.7 68.6 79.1 97.9 0.9 0.6 59.1 2.1 8.9 1.4 4.7 381
ROMANESCO
Amfora 13.0 4.7 16.0 2.9 3.9 0.5 6.3 4.4 1.5 53
Bejo 1955 25.4 3.0 2.1 3.1 3.0 5.4 3.2 1.1 46
Veronica 15.9 3.6 12.4 2.0 3.9 0.2 5.5 3.9 0.9 48
68
Table 1. Continued.
methoxyglucobrassicin
variety
glucoiberin
progoitrin
sinigrine
raphanin
napoleiferin
glucoalysin
gluconapin
4OH-glucobrassicin
glucobrassicanapin
glucobrassicin
gluconasturtiin
4-
neoglucobrassicin
tal to
SAVOY CABBAGE
Ovasa 54.2 17.2 2.7 0.3 15.2 6.1 96
Wirosa 289.8 6.4 141.8 7.8 3.7 27.6 4.7 482
WHITE CABBAGE
Almanac 24.8 28.3 32.2 18.9 18.3 0.9 0.9 2.6 127
Deen 60.7 5.8 106.0 3.8 3.0 0.4 8.3 4.9 1.2 194
Krautman 67.7 6.7 84.1 1.9 4.9 1.4 2.0 1.2 2.6 173
Lennox 109.0 8.2 56.1 18.8 4.3 0.7 3.5 2.5 203
Mandy 100.1 14.6 67.4 28.3 6.3 8.2 1.6 4.0 2.9 233
Mentor 57.6 16.0 142.6 3.1 3.4 10.9 1.6 3.1 2.3 0.4 241
TRONCHUDA
Beira 22.1 1.7 2.1 1.3 4.8 11.7 17.7 3.7 1.6 67
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... It includes important crop species such as Brassica oleracea (e.g., cauliflower, Brussels sprouts, cabbage, broccoli, and Kai Lan), Brassica rapa (e.g., pakchoi, choy sum, and Chinese cabbage), Nasturtium officinale (e.g., watercress), and Raphanus sativus (e.g., daikon radish and red cherry radish). Other species such as Diplotaxis tenuifolia and Eruca vesicaria, commonly referred as 'rocket salads', have also attracted a considerable interest as culinary vegetables because of their strong flavor and content of putative health-promoting compounds (Verkerk et al., 2010). These species and their crop wild relatives (CWR -taxa closely related to crops) grown primarily in the Euro-Mediterranean region, which contains the highest proportion of agronomically important plants representing an important reservoir of genetic resources for crop improvement (Kell et al., 2008). ...
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... "Marathon", purple sprouting broccoli was characterized also by higher levels of glucosinolates. Similarly, Verkerk et al. [232] observed exceptionally high glucoiberin content (396.5 μmol/100 g FW) in purple sprouting broccoli cv "Bordeaux" compared to other green broccoli genotypes, which suggests that there is some sort of interaction between purple pigmentation and glucosinolate profile of broccoli. In another study, analyzing the acylated anthocyanin profile of purple sprouting broccoli and three other green broccoli varieties at the sprouting stage, Moreno et al. [233] observed a significantly higher content of anthocyanins in the purple genotype compared to the green ones and observed that the quantity and quality of anthocyanin pigments were highly variable among the tested genotypes. ...
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