Characterization of Nutritionally Important Carotenoids in Bunching Onion

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  • 1 Plant Sciences Department, The University of Tennessee, 252 Ellington Plant Sciences, 2431 Joa Johnson Drive, Knoxville, TN 37996-4561
  • 2 Department of Agriculture, Illinois State University, Normal, IL 61790
  • 3 North East Regional Plant Introduction Station, USDA-ARS, Plant Genetic Resource Unit, Geneva, NY 14456

Members of the Allium genus are consumed for their culinary flavor attributes, but also contain antioxidant and anticarcinogenic phytochemicals. Bunching onions (Allium fistulosum L.) are commonly used in Asian cuisine, in which both leaves and pseudostems are consumed. Carotenoids and chlorophylls are important classes of phytochemicals gaining attention for their health attributes. The goal of our study was to characterize carotenoids and chlorophylls and identify possible genetic and environmental influences on carotenoid concentrations among A. fistulosum accessions. Twelve USDA-ARS accessions were field grown in Knoxville, TN, and Geneva, NY, during the summer of 2007. After harvest, carotenoid and chlorophyll pigments were evaluated in leaf and pseudostem tissues using high-performance liquid chromatography. We were able to identify the presence of antheraxanthin, β-carotene, chlorophyll a and b, lutein, neoxanthin, and violaxanthin in leaf tissues; however, pigments were not found in pseudostem tissues. Carotenoid and chlorophyll concentrations did not differ among accessions or between locations. It is possible that accessions evaluated in this study were a narrow genetic base or were selected based on flavor attributes and not leaf tissue pigmentation.

Abstract

Members of the Allium genus are consumed for their culinary flavor attributes, but also contain antioxidant and anticarcinogenic phytochemicals. Bunching onions (Allium fistulosum L.) are commonly used in Asian cuisine, in which both leaves and pseudostems are consumed. Carotenoids and chlorophylls are important classes of phytochemicals gaining attention for their health attributes. The goal of our study was to characterize carotenoids and chlorophylls and identify possible genetic and environmental influences on carotenoid concentrations among A. fistulosum accessions. Twelve USDA-ARS accessions were field grown in Knoxville, TN, and Geneva, NY, during the summer of 2007. After harvest, carotenoid and chlorophyll pigments were evaluated in leaf and pseudostem tissues using high-performance liquid chromatography. We were able to identify the presence of antheraxanthin, β-carotene, chlorophyll a and b, lutein, neoxanthin, and violaxanthin in leaf tissues; however, pigments were not found in pseudostem tissues. Carotenoid and chlorophyll concentrations did not differ among accessions or between locations. It is possible that accessions evaluated in this study were a narrow genetic base or were selected based on flavor attributes and not leaf tissue pigmentation.

Allium species have been valued for culinary and medicinal attributes for more than 4000 years. Members of the genus posses therapeutic S-alk(en)yl-L-cysteine sulfoxides (Eady et al., 2008), antibacterial compounds (Kim, 1997), high concentrations of flavonoids, and various antioxidants (Štajner et al., 2006). There has been extensive research into the health properties of bulb onion (Allium cepa L.) and garlic (A. sativum L.); however, little is known about the composition and concentrations of therapeutic compounds in other Allium species. Bunching onion (A. fistulosum L.) is commonly cultivated in China, Korea, and Japan, where it is grown for its foliar tissues and consumed either cooked or as a fresh vegetable (Umehara et al., 2006). With the popularity of Asian cuisine, bunching onions are being consumed more in Western diets.

Carotenoids are lipid soluble pigments integrated into light-harvesting complexes (Croce et al., 1999a, 1999b). Carotenoids function as light-harvesting pigments by channeling photons to the photosynthetic reaction center and functioning as photoprotectants by quenching damaging free radicals or through active nonphotochemical quenching of excess light energy (Croce et al., 1999b; Niyogi, 1999). Carotenoid formation is highly conserved throughout all plant species with six primary functioning carotenoids (antheraxanthin, β-carotene, lutein, neoxanthin, violaxanthin, and zeaxanthin) normally present in leafy tissues (Sandmann, 2001). Carotenoid accumulation in plant tissue is influenced by physiological, biochemical, and genetic factors interacting simultaneously with the growing environment (Chenard et al., 2005; Kopsell et al., 2003, 2004, 2005). Noticeable differences in leaf and fruit tissue colorations among different vegetable species are consistent with differences in carotenoid accumulations and types of carotenoids present (Gross, 1991; Kimura and Rodriguez-Amara, 2003; Sommerburg et al., 1998). Moreover, carotenoid variation among genotypes within species can also be significant (Kopsell et al., 2005; Kurilich et al., 1999).

Associations of increased fruit and vegetable consumption with the prevention of chronic diseases are shedding new light on the roles of chlorophylls as valuable phytochemicals (Ferruzzi and Blakeslee, 2007). Recent evidence is also suggesting that dietary chlorophylls may possess biological activities associated with cancer prevention, antimutagenic activity, and induction of apoptosis in tumor cells (Balder et al., 2006; Egner et al., 2003). Alternatively, dietary chlorophylls may reduce intestinal absorption of potentially harmful chemical mutagens and carcinogens (Hartman and Shankel, 1990; Natsume et al., 2004). Dietary chlorophylls from green vegetables such as bunching onions may soon be recognized for their health properties.

Genetic variability for total carotenoid and chlorophyll pigments among different Allium species has previously been reported (Štajner et al., 2006); however, characterization of individual carotenoids present in the leaf and pseudostem tissues and genetic variations among bunching onion germplasm is lacking. Therefore, the goal of this study was to characterize carotenoid and chlorophyll pigment concentrations among different plant accessions available as germplasm from the USDA-ARS Plant Genetic Resources Unit. This study will identify and quantify carotenoid pigments present in the tissues of bunching onions. Data may be useful for dieticians assessing the nutritional contributions of bunching onions in regard to carotenoids. Data may also be valuable to plant improvement programs designed to increase the nutritional value of onions and allied crops.

Materials and Methods

Plant culture and harvest.

Assessment of tissue carotenoid variability among bunching onion genotypes was performed using 12 USDA-ARS accessions (Table 1). Seeds from each accession were sown and cultured under protected culture using a Cornell Mix described by Boodley and Sheldrake (1977) at the Plant Genetic Resource Unit in Geneva, NY, on 19 Mar. 2007. Seedlings of each accession were shipped to Knoxville, TN, on 23 Apr. 2007.

Table 1.

Mean concentrationsz (mg/100 g fresh weight) for carotenoid pigments in leaf tissues of bunching onion (Allium fistulosum L.) USDA-ARS accessions field-grown in Knoxville, TN, and Geneva, NY.

Table 1.

At the Geneva, NY, location, seedlings were transplanted to the field on 15 May 2007. Transplants were placed 16 cm apart in double rows set 92 cm apart on black plastic covering a Honeoye silt loam soil (fine-loamy, mixed, active, mesic Glossic Hapludalf). Preplant fertilizer applications were 112.1N–43.6P–83.1K (in kg·ha−1 from potassium nitrate, monoammonium phosphate, and muriate of potash). The plot also received two fertigation applications of 14 kg N/ha (as ammonium nitrate) through drip irrigation 14 and 28 d after transplanting. Plots consisted of three individual plants for each accession set in single rows of the plastic and were arranged in a randomized complete block replicated three times.

At the Knoxville, TN, location, seedlings were grown under protected culture and were transplanted to the field on 11 May 2007. Transplants were placed 12 cm apart in double rows set 50 cm apart on black plastic (86.4 cm in width) covering a Sequatchie silt loam soil (fine-loamy, siliceous, thermic Humic Hapudult). Preplant fertilizer and fertigation applications were the same as those described for the Geneva, NY, location. The experimental design was also similar to the Geneva, NY, location. Onions were harvested and all three plants were bulked as one sample on 27 to 28 June in Knoxville, TN, and on 4 to 6 July in Geneva, NY. Plants were stored on ice, transported to the laboratory, and cleaned of any residual soil. The root plate was removed and the plants were divided into pseudostem and leaf tissues at the separation layer between the tissues. Geneva, NY, samples were packed in dry ice and shipped to Knoxville for analysis. All samples were frozen at –80 °C before lyophilization (Model 6L FreeZone; LabConCo, Kansas City, MO).

Tissue extraction.

Tissues were freeze-dried at a constant temperature of –25 °C before extraction. Pigments were extracted from freeze-dried tissues according to Kopsell et al. (2004) and analyzed according to Kopsell et al. (2007a). A 0.1-g tissue subsample was rehydrated with 0.8 mL of ultrapure H2O and placed in a water bath set at 40 °C for 20 min. After incubation, 0.8 mL of the internal standard ethyl-β-8′-apo-carotenoate (Sigma Chemical Co., St. Louis, MO) was added to determine extraction efficiency. The addition of 2.5 mL of tetrahydrofuran (THF) stabilized with 25 mg·L−1 of 2,6-Di-tert-butyl-4-methoxyphenol was performed after sample hydration. The sample was then homogenized in a Potter-Elvehjem (Kontes, Vineland, NJ) tissue grinding tube using ≈25 insertions with a pestle attached to a drill press set at 540 rpm. During homogenization, the tube was immersed in ice to dissipate heat. The tube was then placed into a clinical centrifuge for 3 min at 500 gn. The supernatant was removed and the sample pellet was resuspended in 2 mL THF and homogenized again with the same extraction technique. The procedure was repeated for a total of four extractions to obtain a colorless supernatant. The combined supernatants were reduced to 0.5 mL under a stream of nitrogen gas (N-EVAP 111; Organomation Inc., Berlin, MA) and brought up to a final volume of 5 mL with methanol (MeOH). A 2-mL aliquot was filtered through a 0.2-μm polytetrafluoroethylene filter (Model Econofilter PTFE 25/20; Agilent Technologies, Wilmington, DE) using a 5-mL syringe (Becton, Dickinson and Company, Franklin Lakes, NJ) before high-performance liquid chromatography (HPLC) analysis.

High-performance liquid chromatography pigment analysis.

An Agilent 1200 series HPLC unit with a photodiode array detector (Agilent Technologies, Palo Alto, CA) was used for pigment separation. Chromatographic separations were achieved using an analytical scale (4.6 mm i.d. × 250 mm) 5 μm, 200 Å polymeric RP-C30 column (ProntoSIL, MAC-MOD Analytical Inc., Chadds Ford, PA), which allowed for effective separation of chemically similar pigment compounds. The column was equipped with a 5-μm guard cartridge (4.0 mm i.d. × 10 mm) and holder (ProntoSIL) and was maintained at 30 °C using a thermostatted column compartment. All separations were achieved isocratically using a binary mobile phase of 11% methyl tert-butyl ether, 88.99% MeOH, and 0.01% triethylamine (v/v/v). The flow rate was 1.0 mL·min−1 with a run time of 53 min followed by a 2-min equilibration before the next injection. Eluted compounds from a 10-μL injection were detected at 453 (carotenoids and internal standard), 652 [chlorophyll a (Chl a)], and 665 Chl b) nm and data were collected, recorded, and integrated using ChemStation Software (Agilent Technologies). Peak assignment for individual pigments was performed by comparing retention times and line spectra obtained from photodiode array detection using external standards (β-carotene, Chl a, Chl b, lutein, neoxanthin, violaxanthin, zeaxanthin from ChromaDex Inc., Irvine, CA).

Data sets were analyzed by the GLM procedures of SAS (Cary, NC) with cultivar means separated by least significant difference of α = 0.05. Leaf tissue pigment data are presented on a fresh weight (FW) basis.

Results and Discussion

Leaf tissue carotenoid and chlorophyll pigments were not influenced by growing location or by accession (Tables 1 and 2). The USDA Nutrient Database lists A. fistulosum as averaging 0.60 mg/100 g FW of β-carotene and 1.14 mg/100 g FW of lutein + zeaxanthin (USDA Nutrient Database, 2008). Previously, total carotenoids in the leaf tissues of A. fistulosum (cultivar not reported) were reported to be 2.87 mg·g−1 FW (Štajner et al., 2006). Umehara et al. (2006) reported β-carotene values in the leaves of A. fistulosum L. cv. Kujyoasagikei to be 4.63 mg/100 g FW. Carotenoid values for accessions in the current study differ from values reported previously (Tables 1). These previous reports used different extraction and analytical methods to determine carotenoid concentrations. Our current analytical protocol includes methods proven to be more efficient at tissue pigment separation and detection, which may account for the differences for carotenoid concentrations among the studies (Emenhiser et al., 1995). Leaf tissue pigments were well separated (see Kopsell et al., 2007b for a representative chromatogram); however, pseudostem tissue pigments were below HPLC detection limits. To the best of our knowledge, this is the first study to characterize the major carotenoid pigments present in the leaf tissues of A. fistulosum germplasm.

Table 2.

Mean concentrationsz (mg/100 g fresh weight) for chlorophyll pigments in leaf tissues of bunching onion (Allium fistulosum L.) USDA-ARS accessions field-grown in Knoxville, TN, and Geneva, NY.

Table 2.

Intraspecific genetic variation for leaf tissues carotenoids has been reported for dicot vegetables. Lutein ranged from 4.8 to 13.4 mg/100 g fresh weight and β-carotene ranged from 3.5 to 10.0 mg/100 g fresh weight in Brassica oleracea L. var. acephala (Kopsell et al., 2004). Lutein ranged from 4.2 to 8.3 mg/100 g FW, zeaxanthin ranged from 0.2 to 0.6 mg/100 g FW, and β-carotene ranged from 3.4 to 7.7 mg/100 g FW in Ocimum basilicum L. (Kopsell et al., 2005). Lutein ranged from 6.5 to 13.0 mg/100 g FW and β-carotene ranged from 4.1 to 10.9 mg/100 g FW in Spinacia oleracea L. (Kopsell et al., 2006). Lutein ranged from 0.1 to 5.8 mg/100 g FW and β-carotene ranged from 0.1 to 9.1 mg/100 g FW in Lactuca species (Kimura and Rodriguez-Amaya, 2003; Mou, 2005). Lack of genetic variation for leaf tissue carotenoid among the A. fistulosum accessions in the current study may reflect a narrow genetic pool possibly present in the germplasm held in the repository. The sample size of only 12 accessions may not have been enough to capture variation present within the species. It may also be possible that the germplasm parental material was selected based on flavor attributes and not carotenoid concentrations. Unique metabolism of secondary sulfur metabolites within the Alliums contributes to their intense flavors. Brassica species metabolize sulfur into glucosinolates responsible for flavor intensity. In a previous study, Kopsell et al. (2003) demonstrated that sulfur fertility increases glucosinolate compounds, but did not influence leaf tissue carotenoid accumulations among different B. oleracea L. var. acephala cultivars. Therefore, selections for flavor intensity would not be expected to impact leaf tissue carotenoid accumulations in B. oleracea and possibly A. fistulosum.

Bulb onions are rich sources of flavonoids and S-alk(en)yl-L-cysteine sulfoxides shown to convey beneficial health properties when consumed in the diet. Leaf tissues of Allium species will contain nutritionally important carotenoid and chlorophyll pigments. The current study demonstrates high concentrations of a variety of valuable pigments in leaf tissues of A. fistulosum accessions. These compounds were shown to be similar at two environments and among 12 accessions. Information from this study may be valuable for plant improvement programs, which use this germplasm to develop A. fistulosum or allied crops with higher concentrations of nutraceutical pigments.

Literature Cited

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    • Search Google Scholar
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    • Search Google Scholar
    • Export Citation
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  • Sandmann, G. 2001 Genetic manipulation of carotenoid biosynthesis: Strategies, problems and achievements Trends Plant Sci. 6 14 17

  • Sommerburg, O., Keunen, J.E.E., Bird, A.C. & van Kuijk, F.J.G.M. 1998 Fruits and vegetables that are sources for lutein and zeaxanthin: The macular pigment in human eyes Br. J. Ophthalmol. 82 907 910

    • Search Google Scholar
    • Export Citation
  • Štajner, D., Milić, N., Čanadanović-Brunet, J., Kapor, A., Štajner, M. & Popović, B.M. 2006 Exploring Allium species as a source of potential medicinal agents Phytother. Res. 20 581 584

    • Search Google Scholar
    • Export Citation
  • Umehara, M., Sueyoshi, T., Shimomure, K., Iwai, M., Shigyo, M., Hirashima, K. & Nakahara, T. 2006 Interspecific hybrids between Allium fistulosum and Allium schoenoprasum reveal carotene-rich phenotype Euphytica 148 295 301

    • Search Google Scholar
    • Export Citation
  • USDA Nutrient Database 2008 National Nutrient Database for Standard Reference, Release 21 U.S. Dept. Agr., Agr. Res. Serv. 1 Sept. 2008 22 June 2009 <http://www.nal.usda.gov/fnic/foodcomp/search/>.

    • Export Citation

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Contributor Notes

This research was made possible through support from the University of Tennessee Institute of Agriculture.

Associate Professor.

Professor.

Graduate Research Assistant.

Assistant Professor.

Research Professor.

To whom reprint requests should be addressed; e-mail dkopsell@utk.edu.

  • Balder, H.F., de Vogel, J., Jansen, M.C.J.F., Weijenberg, M.P., van den Brandt, P.A., Westenbrink, S., van der Meer, R. & Goldbohm, R.A. 2006 Heme and chlorophyll intake and risk of colorectal cancer in The Netherlands cohort study Cancer Epidemiol. Biomarkers Prev. 15 717 725

    • Search Google Scholar
    • Export Citation
  • Boodley, J.W. & Sheldrake R. Jr 1977 Cornell peat-lite mixes for commercial plant growing N.Y. State College Agr. Life Sci. Inf. Bull. 43 1 8

  • Chenard, C.H., Kopsell, D.A. & Kopsell, D.E. 2005 Nitrogen concentration affects nutrient and carotenoid accumulation in parsley J. Plant Nutr. 28 285 297

    • Search Google Scholar
    • Export Citation
  • Croce, R., Remelli, R., Varotto, C., Brenton, J. & Bassi, R. 1999a The neoxanthin binding site of the major light-harvesting complex (LHCII) from higher plants FEBS Lett. 456 1 6

    • Search Google Scholar
    • Export Citation
  • Croce, R., Weiss, S. & Bassi, R. 1999b Carotenoid-binding sites of the major light-harvesting complex II of higher plants J. Biol. Chem. 274 29613 29623

    • Search Google Scholar
    • Export Citation
  • Eady, C.C., Kamoi, T., Kato, M., Porter, N.G., Davis, S., Shaw, M., Kamoi, A. & Imai, S. 2008 Silencing onion lachrymatory factor synthase causes a significant change in the sulfur secondary metabolic profile Plant Physiol. 147 2096 2106

    • Search Google Scholar
    • Export Citation
  • Egner, P.A., Munoz, A. & Kensler, T.W. 2003 Chemoprevention with chlorophyllin in individuals exposed to dietary aflatoxin Mutat. Res. 523 209 216

  • Emenhiser, C., Sander, L.C. & Schwartz, S.J. 1995 Capability of a polymeric C30 stationary phase to resolve cis-trans carotenoid isomers in reverse-phase liquid chromatography J. Chromatography 707 205 216

    • Search Google Scholar
    • Export Citation
  • Ferruzzi, M.G. & Blakeslee, J. 2007 Digestion, absorption, and cancer preventative activity of dietary chlorophyll derivatives Nutr. Res. 27 1 12

  • Gross, J. 1991 Carotenoids 75 147 Pigments in vegetables: Chlorophylls and carotenoid AVI/Van Nostrand Reinhold New York, NY

  • Hartman, P. & Shankel, D. 1990 Antimutagens and anticarcinogens: A survey of punitive interceptor molecules Environ. Mol. Mutagen. 5 145 182

  • Kim, J.H. 1997 Anti-bacterial action of onion (Allium cepa L.) extracts against oral pathogenic bacteria J. Nihon Univ. Sch. Dent. 39 136 141

  • Kimura, M. & Rodriguez-Amaya, D.B. 2003 Carotenoid composition of hydroponic leafy vegetables J. Agr. Food Chem. 51 2603 2607

  • Kopsell, D.A., Barickman, T.C., Sams, C.E. & McElroy, J.S. 2007a Influence of nitrogen and sulfur on biomass production and carotenoid and glucosinolate concentrations in watercress (Nasturtium officinale R.Br.) J. Agr. Food Chem. 55 10628 10634

    • Search Google Scholar
    • Export Citation
  • Kopsell, D.A., McElroy, J.S., Sams, C.E. & Kopsell, D.E. 2007b Genetic variation in carotenoid concentrations among diploid and amphidiploid rapid-cycling Brassica species HortScience 42 461 465

    • Search Google Scholar
    • Export Citation
  • Kopsell, D.A., Kopsell, D.E. & Curran-Celentano, J. 2005 Carotenoid and chlorophyll pigments in sweet basil grown in the field and greenhouse HortScience 40 1230 1233

    • Search Google Scholar
    • Export Citation
  • Kopsell, D.A., Kopsell, D.E., Lefsrud, M.G., Curran-Celentano, J. & Dukach, L.E. 2004 Variation in lutein, beta-carotene, and chlorophyll concentrations among Brassica oleracea cultigens and seasons HortScience 39 361 364

    • Search Google Scholar
    • Export Citation
  • Kopsell, D.E., Kopsell, D.A., Randle, W.M., Coolong, T.W., Sams, C.E. & Curran-Celentano, J. 2003 Kale carotenoids remain stable while flavor compounds respond to changes in sulfur fertility J. Agr. Food Chem. 51 5319 5325

    • Search Google Scholar
    • Export Citation
  • Kopsell, D.A., Lefsrud, M.G., Kopsell, D.E., Wenzel, A.J., Gerweck, C. & Curran-Celentano, J. 2006 Spinach cultigens variation for tissue carotenoid concentrations influences human serum carotenoid levels and macular pigment optical density following a 12-week dietary intervention J. Agr. Food Chem. 54 7998 8005

    • Search Google Scholar
    • Export Citation
  • Kurilich, A.C., Tsau, G.J., Brown, A., Howard, L., Klein, B.P., Jeffery, E.H., Kushad, M., Wallig, M.A. & Juvik, J.A. 1999 Carotene, tocopherol, and ascorbate contents in subspecies of Brassica oleracea J. Agr. Food Chem. 47 1576 1581

    • Search Google Scholar
    • Export Citation
  • Mou, B. 2005 Genetic variation of beta-carotene and lutein contents in lettuce J. Amer. Soc. Hort. Sci. 130 870 876

  • Natsume, Y., Satsu, H., Kitamura, K., Okamoto, N. & Shimizu, M. 2004 Assessment system for dioxin absorption in the small intestine and prevention of its absorption by food factors Biofactors 21 375 377

    • Search Google Scholar
    • Export Citation
  • Niyogi, K.K. 1999 Photoprotection revisited: Genetics and molecular approaches Annu. Rev. Plant Physiol. Plant Mol. Biol. 50 333 359

  • Sandmann, G. 2001 Genetic manipulation of carotenoid biosynthesis: Strategies, problems and achievements Trends Plant Sci. 6 14 17

  • Sommerburg, O., Keunen, J.E.E., Bird, A.C. & van Kuijk, F.J.G.M. 1998 Fruits and vegetables that are sources for lutein and zeaxanthin: The macular pigment in human eyes Br. J. Ophthalmol. 82 907 910

    • Search Google Scholar
    • Export Citation
  • Štajner, D., Milić, N., Čanadanović-Brunet, J., Kapor, A., Štajner, M. & Popović, B.M. 2006 Exploring Allium species as a source of potential medicinal agents Phytother. Res. 20 581 584

    • Search Google Scholar
    • Export Citation
  • Umehara, M., Sueyoshi, T., Shimomure, K., Iwai, M., Shigyo, M., Hirashima, K. & Nakahara, T. 2006 Interspecific hybrids between Allium fistulosum and Allium schoenoprasum reveal carotene-rich phenotype Euphytica 148 295 301

    • Search Google Scholar
    • Export Citation
  • USDA Nutrient Database 2008 National Nutrient Database for Standard Reference, Release 21 U.S. Dept. Agr., Agr. Res. Serv. 1 Sept. 2008 22 June 2009 <http://www.nal.usda.gov/fnic/foodcomp/search/>.

    • Export Citation
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