Research Article

Korean Journal of Plant Resources. 1 December 2021. 575-599
https://doi.org/10.7732/kjpr.2021.34.6.575

ABSTRACT


MAIN

  • Introduction

  • Materials and Methods

  •   Plant cultivation and sample preparation

  •   Characterization of phenotypic traits

  •   Evaluation of glucosinolate contents

  •   Free-radical scavenging activity

  •   Statistical analysis

  • Results

  •   Phenotypic traits of radish root

  •   Glucosinolate contents of radish roots

  •   Correlation analysis of phenotypic traits and glucosinolate profiles

  •   Principal component analysis

  •   Glucosinolate contents of root color-based groups

  • Discussion

Introduction

The edible roots of radish (Raphanus sativus L., 2n = 2x = 18), a representative of the Raphanus genus in the Brassicaceae family, are consumed worldwide. Radish sprouts and young leaves are also cooked, preserved by salting or pickling, or eaten in salads. According to Vavilov et al. (1926), radish originated from the eastern Mediterranean region and Middle East, and the current varieties might have been domesticated in India and other parts of Asia. Radish has been cultivated in Korea and China since 400 BC (Kaneko and Matsuzawa, 1993; Kurina et al., 2021; Vavilov et al., 1926). Historical reports of radish kimchi date back to the Three Kingdoms era (700 BC) in Korea, and traditional radish recipes have been published in at least 11 Korean recipe books within the past 100 years (Cho, 2010). Radish is one of the most widely cultivated vegetables in Korea and has been professionally bred for “four-season cultivation”.

In Asian countries, diverse varieties of radish are widely cultivated as large-rooted and long-season vegetables, whereas in the Americas and Europe, red, small-rooted, short-season radish varieties are cultivated. Black radish is used in salads in Spain because of its crispy texture, and in China, colorful radishes including 20-day red radish, green radish (green both outside and inside the root), and watermelon radish (green exterior and red interior) are consumed (Singh et al., 2017; Vavilov et al., 1926; Wang et al., 2020). In contrast to the colorful radishes cultivated in China, white radishes with green shoulders have been preferred in Korea for a long time because there is a perception that these types of radishes, especially egg-shaped ones, are of higher quality, being sweet and crunchy. Most radish and Brassica spp. researches conducted in Korea have focused on cultivation and disease resistance (Afroz et al., 2021; Geum et al., 2021; Kim et al., 2020; Kwon et al., 2020; Rajalingam et al., 2021), with few studies conducted on the color and appearance of radish roots (Singh et al., 2017). However, color is one of the most important traits reflecting quality, and affects consumer preference.

Glucosinolates (GSLs) are sulfur-containing secondary metabolites considered as the main health-promoting (anti-cancer, antioxidant, and anti-inflammatory) compounds in most cruciferous vegetables (Barillari et al., 2005). GSLs have been reported in various species and cultivars, as well as in specific plant organs (Hwang et al., 2019; Jeon et al., 2018; Rhee et al., 2020). Glucoraphasatin (GRH), which is derived from glucoerucin (GER), is abundant in radish (Fahey et al., 2001; Ishida et al., 2015; Kakizaki et al., 2017). Rhee et al. (2020) assessed the GSL distribution across the inner, middle, and outer leaves of kimchi cabbage (Brassica rapa L.), and Jeon et al. (2018) evaluated the GSL content at different vegetative growth stages in B. rapa (Jeon et al., 2018; Rhee et al., 2020).GSLs can be hydrolyzed by myrosinase to form breakdown products including isothiocyanates, which are responsible for the bitter taste of vegetables and exhibit cancer chemopreventive activity. Liu et al. (2018) compared nutritional values among different broccoli tissues and suggested various possible applications for broccoli by-products after analyzing sulforaphane derived from glucoraphanin (Liu et al., 2018). GRH is hydrolyzed by myrosinase when plant cells are disrupted to produce raphasatin; when derived from GRH, raphasatin was reported to induce more potent detoxification enzymes than other degradation products (Scholl et al., 2011). Raphasatin exhibits chemopreventive effects, including some toxic effects on human breast adenocarcinoma cells (Scholl et al., 2011; Suzuki et al., 2016; 2017), in which it induces apoptosis (Ibrahim et al., 2018). Radish also converts isothiocyanates from GSLs more efficiently than broccoli (De Nicola et al., 2013), with the addition of radish sprouts to broccoli sprouts promoting sulforaphane formation in the latter (Liang et al., 2018). Therefore, it is important to identify radish varieties that produce large amounts of GSLs, as they can provide health benefits to humans.

Montaut et al. (2010) provide an excellent summary of GSL analytical methods (Montaut et al., 2010). High-performance liquid chromatography (HPLC) has been used in many studies (Park et al., 2014) to analyze desulfated GSL with a UV-visible or photodiode array detector, but the desulfonation process is laborious, and some GSL may be insufficiently desulfonated at lower sulfatase concentrations. Recently, intact GSLs were identified and quantified using ultra- performance liquid chromatography (UPLC) with diode array detection-tandem mass spectrometry (MS/MS) in multiple reaction monitoring (MRM) mode (Gratacós-Cubarsí et al., 2010; Hwang et al., 2019). Several studies have analyzed GSL contents in the Brassicaceae family (Bhandari et al., 2015), but they often did not include GRH, which comprises 90% of all radish GSLs on average. Yi et al. (2016) investigated radish GSLs, but the numbers of germplasms and morphological traits analyzed were limited, and GSLs were analyzed in the form of desulfo-GSLs using HPLC (Yi et al., 2016).

Large-scale characterization and evaluation of the agronomic traits and health-promoting chemicals in radish germplasms would help identify new germplasm breeding materials. Therefore, in this study, we aimed to profile GSLs and characterize the phenotypes of radish germplasms. We evaluated the GSL contents of 110 radish germplasms using liquid chromatography (LC)-MS/MS in MRM mode, and characterized qualitative and quantitative traits. The data from the correlation analysis could promote the exploitation of favorable traits by breeders, as well as diet diversification given the health benefits associated with various radish germplasms.

Materials and Methods

Plant cultivation and sample preparation

Seeds of 110 radish germplasms were obtained from the National Agrobiodiversity Center (Jeonju, Korea), and seeds of the following 10 Korean commercial cultivars were purchased from various companies: Gwailmu (Con1; Asia Seed Co., Seoul, Korea), Meosjinmaskkalmu (Con2; Nongwoobio., Suwon, Korea), Taecheong (Con3; Syngenta, Iksan, Korea), Cheong- unmu (Con4; Farm Hannong, Seoul, Korea), Chorongmu (Con5; Farm Hannong), Mansa-hyeongtongmu (Con6; Nongwoobio.), Togwanggoldeumu (Con7; Farm Hannong), Baeksinaltari (Con8; Koregon, Seoul, Korea), Syupeogiljomu (Con9; Nongwoobio.), and Seohogoldeumu (Con10; Nongwoobio.; Appendix 1).

The seeds were sown in an experimental field containing compost and fertilizer at the end of August 2017. Plants were cultivated in the field following cultural practices recommended by the Rural Development Administration. Fertilizer (N-P-K-Ca-B = 60-40-60-75-1.5 ㎏/10 a) was applied before the seeds were sown. Radishes were harvested at 3-10 weeks after sowing (at the optimal growth stage) for phenotypic characterization, and all root samples were freeze-dried (LP500 vacuum freeze-drier; Ilshinbiobase Co., Seoul, Korea) directly at -70℃ for 1 week. The samples were then ground into fine powder and stored at -20℃ until further analysis.

Characterization of phenotypic traits

Phenotypic traits were characterized at full maturity in the field. Radish leaves and roots were examined for 5 qualitative and 10 quantitative traits based on modified descriptors from the International Union for the Protection of New Varieties of Plants (UPOV, 2021) and reference descriptors for Brassica and Raphanus (IBPGR, 1990).

The five qualitative traits were radish root peel color, root shoulder color, root flesh color, root shape, and the extent of root burial in soil. The 10 quantitative traits were total weight (Twe), root length (RL), root width (Rwi), root length-to- width ratio (RR), root weight (Rwe), leaf length (LL), leaf width (Lwi), leaf length-to-width ratio (LR), leaf weight (Lwe), and leaf number (LN). Each characteristic was examined using a digital caliper and digital balance. Three to five independent biological samples were examined to characterize the quantitative and qualitative phenotypic traits.

Evaluation of glucosinolate contents

GSLs were extracted following the method reported by Rhee et al. (2020). GSLs were isolated from 100-mg freeze-dried samples using 1 mL of solvent (Methanol: deionized water = 80:20, v/v). Then, each mixture was vortexed and centrifuged at 16,000 rpm and 4℃ for 10 min. The supernatant was transferred into a new tube, re-centrifuged, filtered using a 0.45-㎛ syringe filter, and diluted 10 times before an internal standard solution was added. Finally, the filtered solution was transferred into a brown vial for further analysis. For this experiment, the internal standard was prepared using 100 ppb glucotropaeolin. We analyzed 18 GSL standards (Phytoplan Diehm & Neuberger GmbH; Heidelberg, Germany) using a Waters Acquity UPLC system (Waters, Milford, MA, USA) coupled with a Xevo TQ-S system (Waters MS Technologies, Manchester, UK) and finally selected the following five GSLs to evaluate the GSL contents in radish germplasms (Appendix 4): Glucoraphasatin (GRH), glucoraphenin (GRE), glucobrassicin (GBR), Glucoerucin (GER), and glucoberteroin (GBE). Glucotropaeolin was used as the internal standard to identify and quantify the GSLs in 110 germplasms and 10 commercial cultivars. Chromatographic separation was carried out using an Acquity UPLC BEH C18 (1.7 ㎛, 2.1 × 100 ㎜) column (Waters Corp., Manchester, UK). The flow rate was kept at 0.25 mL/min, the column temperature was maintained at 35℃, and the injection volume was 5 μL. The mobile phase comprised 0.1% trifluoroacetic acid in distilled water (A) and 0.1% trifluoroacetic acid in methanol (B). The UPLC gradient conditions were as follows: initial condition, 100% A; 0.0-1.0 min, 100% to 95% A; 1.0-4.0 min, 95% to 0% A; 4.0-4.5 min, 0% to 100% A; 4.5-5 min, 100% A; 5-15 min, 100% A. The mass spectrometry instrument was operated in negative ion electrospray ionization (ESI) and MRM modes. Data were acquired using MassLynx 4.1 software. GSLs were identified by comparing their retention times and MS and MS/MS fragmentation spectra with those of commercial standards. Each MRM transition was set as follows {compound name (retention time, parent molecular weight > daughter transition weight)}: GRH (5.18 min, 417 > 175.69), GRE (6.21 min, 433 > 418.5), GER (4.87 min, 419 > 177.71), GBE (6.21 min, 433 > 127.78), GBR (5.51 min, 446 > 204.69), and glucotropaeolin (4.75 min, 407 > 165.94). The final concentration of each GSL was calculated based on its curve area relative to that of the internal standard (glucotropaeolin) and linear regression equations derived from the calibration curve of the corresponding standard. The final concentrations of individual GSLs are presented in units of ㎍/g sample dry weight (DW).

Free-radical scavenging activity

To evaluate antioxidant activity in the radish germplasms, we modified the 2,2-diphenyl-1-picrylhydrazyl (DPPH) test protocol of Brand-Williams et al. (1995). DPPH powder (Sigma-Aldrich, St. Louis, MO, USA) was dissolved in 200 mL methanol to make a 150 mM DPPH solution, which was shaken in the dark for 1 h. Then, 1 mL of 80% methanol was added to each 2-mg freeze-dried sample, and the mixture was sonicated for 1 h and then centrifuged. The supernatant was analyzed for antioxidant activity. For the analysis, 150 μL of 150 mM DPPH and 100 μL of 2,000 ppm sample extract were mixed. DPPH solution and ascorbic acid (Sigma-Aldrich, Milwaukee, WI, USA) were used as a blank and standard, respectively. The absorbance at a wavelength of 517 ㎚ was measured. Experiments were performed in triplicate with independent germplasms. The free-radical scavenging activity was calculated as follows:

DPPH free-radical scavenging activity (%) = [1 - (A sample - A sample blank) / (A control - A control blank)] × 100%, where A is the absorbance at 517 ㎚.

Statistical analysis

All experiments of GSL contents were conducted in technical triplicate, and the average ± standard deviation of GSL contents were calculated (㎍/g of root DW). Correlation analysis of the 10 phenotypic traits and individual and total compound amounts, as well as principal component analysis (PCA) of GSL contents and free-radical scavenging activities, were performed using XLSTAT software (Addinsoft, Paris, France). Analysis of variance followed by Duncan’s multiple range test {least significant range (LSR), p < 0.05} was performed to determine if the content of each compound varied significantly by phenotypic traits. Student’s t-test was done to identify significant-phenotypic differences between germplasms and cultivars.

Results

Phenotypic traits of radish root

In total, 15 phenotypic traits important for radish breeding were evaluated, including root color, shape, weight, and length. Five qualitative and ten quantitative traits of 110 radish germplasms and 10 Korean commercial cultivars were assessed (Appendix1 and 2), and the results are summarized in Table 1 and 2. Broad variation in all qualitative traits was observed in the radish germplasms compared to the commercial cultivars. In the latter, there was relatively little variation, especially in root peel color and root shoulder color. The root peel color of most germplasms (70.9%) and all cultivars (100%) was white. For the rest of the germplasms, two other root peel colors, bronze-green and red, were dominant. The radish germplasms produced roots with various root shoulder colors, including green (31.8%), whereas only the green shoulder color was observed in the cultivars. The root flesh color in the germplasm-produced roots and cultivars was mainly white (77.3% and 90%, respectively). Nineteen germplasms, but no cultivars, produced roots with green flesh. The germplasms produced various root shapes, such as a narrow rectangle (31.8%), sphere (19.1%), and rectangle (17.3%), whereas the roots of the cultivars were mostly elliptical (70%) or gourd- shaped (20%). Regarding the root position in soil, germplasm- produced roots were mostly buried (46.4%) or half buried (30.9%), whereas most cultivar-produced roots were half buried in soil (60%).

Table 1.

Qualitative traits of 110 radish germplasms and 10 commercial cultivars, as evaluated using modified and reference UPOV (2021) and IBPGR (1990) descriptors, respectively, for Brassica and Raphanus

No. Phenotypic traits Description Germplasms Cultivars
n % n %
1 Root peel color Bronze-green 19 17.3 0 0
Red 13 11.8 0 0
White 78 70.9 10 100
2 Root shoulder color Bronze-green 19 17.3 0 0
Red 13 11.8 0 0
Green 35 31.8 10 100
White 43 39.1 0 0
3 Root fresh color Red 6 5.5 1 10
Green 19 17.3 0 0
White 85 77.3 9 90
4 Root shape Almond 5 4.5 0 0
Ovate 13 11.6 0 0
Gourd 1 0.9 2 20
Narrow rectangle 35 31.8 0 0
Elliptic 4 3.6 7 70
Rectangle 19 17.3 0 0
Spheerical 21 19.1 0 0
Transverse elliptic 4 3.6 0 0
Broad rectangle 8 7.3 1 10
5 Root position in soil Above 6 5.5 0 0
Mostly above 19 17.3 1 10
Half buried 34 30.9 6 60
Mostly buried 51 46.4 3 30
Sum 110 10

Quantitative traits were more variable in the radish germplasms compared to the cultivars, especially Twe, Rwe, Lwe, RL, LL, Rwi, Lwi, RR, LR, and LN (Table 2). The average Twe of the cultivars was higher (2,088.9 g) than that of the germplasms (1,827.5 g), as was the average Rwe (1,753.3 vs. 1,286.3 g). Conversely, the average Lwe of the germplasms was higher (541.1 g) than that of the cultivars (335.3 g), and the average RL and LL were greater in the germplasms (24.1 and 45.6 ㎝, respectively) than in the cultivars (20.6 and 39.9 ㎝, respectively), despite the average Rwi (11.8 vs. 10 ㎝) and Rwe being greater in the latter. Both Rwe and Lwe were significantly different between germplasms and cultivars (p < 0.05) in Table 2. Leaves derived from the germplasms were wider (average width, 16.7 ㎝) than in the cultivars (average, 15.9 ㎝), but the LR was similar between the germplasms (2.8) and cultivars (2.5). For the RR, there was a marked difference between the germplasms (2.7) and cultivars (1.7). The numerical difference in the ratio was small, but the RR range of the germplasms was much broader than that of the cultivars. The average LN was similar between the germplasms (26.5) and cultivars (25.1), with the former having a broader range (8.7-59) compared to the latter (19-33).

Table 2.

Quantitative traits of 110 radish germplasms and 10 commercial cultivars. Total weight was calculated as the sum of root weight and leaf weight. The root and leaf ratios are the ratios of root length (㎝) to root width (㎝) and leaf length (㎝) to leaf width (㎝), respectively

No. Phenotypic traits Germplasms Cultivars
Range Median Average ± SDz Range Median Average ± SDz
1 Total weight (Twe; g) 45.4 – 3420.0 1799.1 1827.5 ± 637.8 723.3 - 2776.7 2113.3 2088.7 ± 621.2
2 Root weight (Rwe; g)*y 45.0 - 2918.3 1280.0 1286.3 ± 463.8 588.3 - 2363.3 1948.3 1753.3 ± 529.4
3 Leaf weight (Lwe; g)*y 0.4 - 1833.3 515.2 541.1 ± 279.0 135.0 - 575 363.3 335.3 ± 129.5
4 Root length (RL; ㎝) 2.5 – 48.0 23.2 24.1 ± 10.8 12.0 - 25.8 21.2 20.6 ± 4.6
5 Root width (RW; ㎝) 2.1 - 41.8 9.6 10.0 ± 3.8 10.5 - 12.6 11.8 11.8 ± 0.6
6 Leaf length (LL; ㎝) 14.2 – 62.0 46.8 45.6 ± 8.9 32.3 - 48.3 38.5 39.9 ± 4.6
7 Leaf width (LW; ㎝) 8.4 - 25.8 17.1 16.7 ± 3.3 11.8 - 18.9 17.3 15.9 ± 2.3
8 Root ratio (RR; len/wid) 0.7 - 6.2 2.3 2.7 ± 1.5 1.1 - 2.1 1.9 1.7 ± 0.3
9 Leaf ratio (LR; len/wid) 1.7 - 4.1 2.8 2.8 ± 0.5 2.0 - 3.1 2.5 2.5 ± 0.4
10 Leaf number (LN) 8.7 – 59.0 25.3 26.5 ± 11.0 19.0 – 33.0 25.4 25.1 ± 4.4

zSD means standard deviation, yAsterisk indicates significant differences in each quantitative trait between germplasms and cultivars (t-test, p < 0.05).

Glucosinolate contents of radish roots

The total GSL content and content of each of the five individual GSLs examined in the radish germplasms and cultivars (Appendix 3) are summarized in Table 3. The average total GSL content in the germplasm-produced roots was 7,535.7 ㎍/g DW. The average content of GRH, the main constituent (73.2%) of the total GSL content in radish, was 5,512.9 ㎍/g DW. The GRH content also varied the most widely among the five GSLs (123.8-12,922.0 ㎍/g DW). The average contents of GRE, GER, GBR, and GBE in the germplasm- produced roots were 1,716.9, 165.8, 127.1, and 12.9 ㎍/g DW, respectively. The GBE, GBR and GER contents did not differ significantly from each other, whereas the GRE, GRH, and total GSL contents differed significantly from the contents of the other constituents (Duncan’s LSR, p < 0.05). The GBE, GBR, GER, and GRE contents were similar to each other in the cultivar-produced roots, whereas the GRH and total GSL contents were significantly different from the contents of the other constituents (Duncan’s LSR, p < 0.05). The GRE and GBE contents were significantly different between germplasm-and cultivar-produced roots (Student’s t-test, p < 0.05) in Table 3.

Table 3.

Contents of total glucosinolates (GSLs) and five GSLs in the germplasms and cultivars with the highest contents, mean total and individual GSL contents, and the range of values for each GSL type (㎍/g DW). GSLs contents were analyzed using liquid chromatography-tandem mass spectroscopy in multiple reaction monitoring mode, with glucotropaeolin as the internal standard

110 germplasms 10 commercial varieties
Average Range Top germplasm Average Range Top variety
Total glucosinolate content 7535.7dy 154.3 - 18438.5 299453 7989.6cy 4093.5 - 10873.1 Seohogoldeumu
Glucoraphasatin 5512.9cy 123.8 - 12922.0 215011 6794by 2531.3 - 9247 Seohogoldeumu
Glucoraphenin*z 1716.9by 26.3 - 5653.2 306869 956.8ay 509.6 - 1307.1 Syupeogiljomu
Glucoerucin 165.8ay 2.4 - 534.5 299453 155.4ay 40.9 - 292.9 Gwailmu
Glucobrassicin 127.1ay 0.7 - 1243.9 306869 73.6ay 7.9 - 268.4 Seohogoldeumu
Glucoberteroin*z 12.9ay 0 (ND) - 59.1 299453 9.8ay 4.7 - 17.3 Seohogoldeumu

zAsterisk indicates significant differences in the content of a given compound between germplasms and cultivars (t-test, p < 0.05).

yDifferent characters indicate significant differences in mean content (Duncan’s multiple comparison test, p < 0.05) for each germplasm or cultivar. The glucoraphenin and glucoberteroin contents differed significantly between germplasms and cultivars. No significant differences were found for the other GSLs.

The roots of the following germplasms contained the highest amounts of the specified GSLs (Table 3): IT215011, GRH; IT306869, GRE and GBR; IT299453, GER and GBE. Among the 10 cultivars, Seohogoldeumu had the highest total GSL content (and the highest GRH, GBR, and GBE contents), while Syupeogiljomu had the highest GRE content and Gwailmu had the highest GER content. The content range for all GSLs was broader in germplasm-produced roots than Korean cultivar-produced roots.

Correlation analysis of phenotypic traits and glucosinolate profiles

Correlation analysis of the 15 phenotypic traits and contents of the individual GSLs was performed using XLSTAT software. The Pearson correlation coefficients are presented in Table 4. Twe, which was calculated by summing Rwe and Lwe, was more strongly correlated with Rwe (r = 0.916) than with Lwe (r = 0.725). Twe was also significantly correlated with LL (r = 0.651), RL (r = 0.580), and LN (r = 0.529). Rwe was significantly correlated with RL (r = 0.585), and Lwe was significantly correlated with LL (r = 0.684) and LN (r = 0.629). The RR was more strongly correlated with RL (r = 0.918) than with Rwi (r = -0.463). The RL was negatively correlated with DPPH antioxidant scavenging capacity (r = -0.431). LL was significantly correlated with Lwi (r = 0.678).

Table 4.

Pearson correlation analysis of 10 phenotypic traits and the contents of six GSLs (plus the total GSL content) in 110 germplasms using a range-scaled data set (the minimum and maximum values of normalized data for all traits are 0 and 1, respectively)

Traits Twez Rwe Lwe RL Rwi RR LL Lwi LR LN GRH GRE GBR GER GBE TG
Rwey 0.92**g
Lwex 0.73**g 0.39**g
RLw 0.58**g 0.59**g 0.33**g
Rwiv 0.32**g 0.37**g 0.11 -0.16
RRu 0.33**g 0.28**g 0.28**g 0.92**g -0.46**g
LLt 0.65**g 0.47**g 0.68**g 0.14 0.30**g 0.01
Lwis 0.48**g 0.35**g 0.49**g 0.07 0.23*gh -0.02 0.68**g
LRr 0.25**g 0.18 0.26**g 0.10 0.11 0.03 0.45**g -0.33**
LNq 0.53**g 0.34**g 0.63**g 0.45**g -0.05 0.42**g 0.25**g -0.06 0.38**g
GRHp 0.35**g 0.30**g 0.29**g 0.21*gh 0.07 0.16 0.27**g 0.18 0.13 0.22*gh
GREo 0.18 0.23*gh 0.02 0.06 0.17 -0.02 0.17 0.16 0.04 -0.13 0.76**g
GBRm -0.11 -0.09 -0.10 -0.20*gh 0.06 -0.17 0.07 0.08 0.02 -0.13 0.49***f 0.59**g
GERl 0.32**g 0.31**g 0.20*gh 0.23*gh 0.06 0.17 0.19*gh 0.10 0.12 0.20*gh 0.94**g 0.74**g 0.49**g
GBEk 0.18 0.17 0.11 0.12 0.03 0.11 0.20*gh 0.14 0.10 0.01 0.86**g 0.76**g 0.55**g 0.89**g
TGj 0.31**g 0.29**g 0.23*gh 0.17 0.10 0.12 0.25**g 0.18 0.11 0.13 0.98**g 0.86**g 0.57**g 0.93**g 0.88**g
DPPHi -0.39**g -0.35**g -0.29**g -0.43**g -0.03 -0.38**g -0.26**g -0.17 -0.16 -0.28**g -0.10 -0.01 0.17 -0.15 -0.10 -0.08

Bold characters: r > 0.6, p < 0.01. zTwe: total weight (g), yRwe: root weight (g), xLwe: leaf weight (g), wRL: root length (㎝), vRwi: root width (㎝), uRR: root length-to-width ratio, tLL: leaf length (㎝), sLwi: leaf width (㎝), rLR: leaf length-to-width ratio, qLN: leaf number, pGRH: glucoraphasatin, oGRE: glucoraphenin, mGBR: glucobrassicin, lGER: glucoerucin, kGBE: glucoberteroin, jTG: total GSL content, including GRH, GRE, GBR, GER, and GBE, iDPPH: 2,2-diphenyl-1-picrylhydrazyl. h*, g** and f*** indicate significant correlations between two traits at p < 0.05, p < 0.01 and p < 0.001, respectively.

In Table 4, GRH was significantly correlated with the other GSLs, except GBR. GRH, the most abundant GSL in radish root, was highly correlated with the total GSL content (r = 0.984) and GER (r = 0.938). The strongest correlation among the five GSLs was observed between GRH and GER (r = 0.938), in accordance with previous reports. GRH was also strongly correlated with GBE (r = 0.858) and GRE (r = 0.755). GER (r = 0.934) and GBE (r = 0.878) were more strongly correlated with the total GSL content than was GRE (r = 0.755). GBR had weaker correlations with the other GSLs but was the only GSL positively correlated with DPPH anti-oxidant scavenging (r = 0.166).

Principal component analysis

Principal component analysis was conducted to analyze the relationships among GSL profiles (total GSL content, GRH, GBR, GER, GBE, and GRE) and antioxidant activity (DPPH scavenging) in the 110 radish germplasms (Fig. 1). The first two principal components (F1 and F2), represented as the x- and y-axis in the PCA biplot (Fig. 1), explained 68.88% and 15.97% (sum, 84.85%) of the total variance, respectively.

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Fig. 1.

Principal component analysis (PCA) biplot of root samples produced by 110 radish germplasms based on glucosinolate (GSL) contents and quantitative antioxidant activity. GRH: glucoraphasatin, GRE: glucoraphenin, GER: glucoerucin, GBR: glucobrassicin, GBE: glucoberteroin, TG: total GSL content, DPPH: antioxidant activity.

Five components, namely the total GSL content (20.1%), GRH (18.8%), GER (18.5%), GBE (17.8%), and GRE (15.9%), were the main contributors to F1, whereas DPPH activity (78.8%) and GBR (17.5%) were the main contributors to F2. The six GSL components had positive loadings on F1, with the total GSL content and GRH having the highest loadings, whereas DPPH activity was negatively loaded. DPPH activity, GBR, and GRE had positive loadings on F2, and the total GSL content, GBE, GRH, and GER had negative loadings (Fig. 1).

Based on their location in the PCA plot, the GSL contents may share some common tendencies. Along F1, more positive values reflect higher total GSL, GRH, GER, GBE, and GRE contents, and vice versa. These components do not make a large contribution to F2. More positive values for both F1 and F2 reflect higher GBR content. When the F1 value is positive and the F2 value is negative, the GBR content is low. When the F1 value is negative, the GBR content is intermediate. A negative F1 value and positive F2 value reflects high DPPH activity. In contrast to F2, DPPH activity does make a large contribution to F1, so observations located in the upper half of the plot indicate high DPPH activities and vice versa.

In the PCA biplot, the 110 germplasms were separated into five groups (Fig. 1). Group I (circled in red) contains five radish germplasms (4.5%) and is located in the upper right quadrant between +3.9 and +6.5 on the F1 axis and -0.4 and +2.8 on the F2 axis. The germplasms in Group I had > 10,000 ㎍/g DW GRH, > 15,000 ㎍/g DW for the total GSL content, > 100 ㎍/g DW GBR, and relatively high total GSL and GRH contents compared to the other groups. Two accessions, IT299453 (No. 104) and IT306869 (No. 107), had high total GSL content (18,438 and 18,018 ㎍/g, respectively) but exhibited low and moderate levels of DPPH activity, respectively. IT299453 (No. 104) was also located below IT306869 (No. 107). The IT215011 (No. 36) germplasm had the highest GRH content (12,922 ㎍/g DW) but only a moderate GBR content, and also exhibited moderate DPPH activity. It is positioned on the left side (negative F2) of the plot. Both IT306869 (No. 107) and IT215011 (No. 36) had high total GSL and GRH contents, with moderate levels of DPPH activity.

Group II contains three radish germplasms (2.7%) and is located in the upper right quadrant of the plot, within +0.9 to +1.7 on the F1 axis and +1.5 to +2.8 on the F2 axis (Fig. 1). The germplasms in Group II had total GSL contents of > 9,500 ㎍/g DW and antioxidant activities of > 40%. The GRE and GBR contents were moderate to high. The GSL contents were lower compared to Group I, but the antioxidant activities were higher. Of the three germplasms, IT262036 (No. 71) had the highest GBR content (533.3 ㎍/g DW), and its position indicates an association with GBR-related variables. IT297120 (No. 100) also had a high GBR content (449.1 ㎍/g DW), but its total GSL content was low (although its DPPH activity was still high). IT250790 (No. 53) had a high GRE content (4,421.2 ㎍/g DW).

Group III contains three germplasms and is located within -1.3 to -0.2 on the F1 axis and +2.3 to +3.9 on the F2 axis (Fig. 1). The germplasms in Group III exhibited high antioxidant activities (> 40%, with the highest activity level being 63.1%), moderate-to-low GSL contents, and high GBR contents (> 100 ㎍/g DW). Of the three germplasms, IT264178 (No. 80) exhibited the highest DPPH antioxidant activity but had a low GSL content; IT278682 (No. 84) had the highest GBR content (591.2 ㎍/g) in the group.

Group IV contains 34 germplasms, and is located within -3 to -1.7 on the F1 axis and -1.8 to +3.0 on the F2 axis (Fig. 1). Group IV members had low individual and total GSL contents. Group IV was further divided into three subgroups (Groups i- iii) with 3, 28, and 3 accessions, respectively, according to the antioxidant activity level. Group i members exhibited the highest antioxidant activities (> 45%), followed by Group ii (15-38%) and Group iii members (< 13%). The antioxidant activity levels in Group i were high, although the GSL contents were not. IT278727 (No. 88), IT136498 (No. 22), and IT208400 (No. 31) produced radish roots with red peel. IT208400 (No. 31) exhibited the highest antioxidant activity (59.8%) despite having a low total GSL content (1,334 ㎍/g DW). Group ii members had low GSL contents and exhibited largely similar levels of antioxidant activity. Group iii members {IT103811 (No. 14), IT112253 (No. 16), and IT278685 (No. 87)} exhibited the lowest antioxidant activities (< 13%) and did not produce red roots. IT278685 (No. 87) exhibited the lowest antioxidant activity (4.3%) and had the lowest GSL content.

Group V is positioned in the center of the plot, within -1.7 to +3.5 on both the F1 and F2 axis, and contains 65 germplasms (Fig. 1). No individual traits obviously characterized the group members, and the values of most traits were in the moderate range. To distinguish this group more precisely, more traits need to be analyzed.

Glucosinolate contents of root color-based groups

We classified radish germplasms based on their root color phenotypes, as follows: color group 1, red peel with a red shoulder and white flesh; color group 2, white peel with a green shoulder and red flesh; color group 3, bronze-green peel and shoulder with green flesh; color group 4, white peel, shoulder, and flesh (totally white); and color group 5, white peel with a green shoulder and white flesh (Fig. 2).

/media/sites/kjpr/2021-034-06/N0820340609/images/kjpr_34_06_09_F2.jpg
Fig. 2.

Radish germplasms grouped depending on root colors. Top: The pictures show the exterior and interior of roots containing the highest levels of GSLs for each color group (Nos. 12, 71, 104, 107, and 36). Bottom: The mean total and individual GSL contents in the five color groups. The total (TG) and individual GSL contents and DPPH activity were assessed in multiple comparison tests (Duncan’s least significant range test) to determine if the differences between pairs of color groups were significant (p < 0.05). zTG: total GSL content, yGRH: glucoraphasatin, xGRE: glucoraphenin, vGER: glucoerucin, wGBR: glucobrassicin, uGBE: glucoberteroin. tDifferent characters mean statistically significance.

Color group 1 included 13 germplasms with a mean total GSL content of 4,424.2 ㎍/g DW (range: 642.0-13,044.0 ㎍/g DW; Fig. 2), which was the lowest mean content among all color groups. Color group 2 included six germplasms with a mean total GSL content of 7,082.3 ㎍/g DW (range: 2,660.9- 11,859.5 ㎍/g DW). Color group 3 included 19 germplasms with a mean total GSL content of 9,864.9 ㎍/g DW (range: 1,532.8-18,438.5 ㎍/g DW), which was the highest mean content among all color groups. Color group 4 included 43 germplasms with a mean total GSL content of 7,356.2 ㎍/g DW (range: 154.3-18,017.9 ㎍/g DW), and color group 5 included 29 germplasms with a mean total GSL content of 7,764.3 ㎍/g DW (range: 274.4-16,073.8 ㎍/g DW).

Images above the bar graph show the exterior and interior of the roots in each group with the highest GSL contents (IT102560, IT262036, IT299453, IT306869, and IT215011). In color group 1, the mean GRH, GRE, GBR, GER, and GBE contents were, respectively, 3,214.3, 10,613, 62.43, 81.13, and 5.23 ㎍/g DW, comprising 72.7%, 24%, 1.4%, 1.8%, and 0.1% of the total GSL content. Of the five color groups, group 1 germplasms had the lowest individual GSL contents, but the antioxidant activity was not as low. We further divided this group into two subgroups based on a root weight cutoff of 250 g. Of 13 germplasms, four weighed less than 250 g; these small radishes are eaten in salads or as pickles in Europe and the United States. The small radishes had lower GSL contents compared to the bigger radishes, but the antioxidant activities were high.

In color group 2, the mean GRH, GRE, GBR, GER, and GBE contents were, respectively, 4,928.7, 1,690.7, 364.9, 90.8, and 7.2 ㎍/g DW, comprising 69.6%, 23.9%, 5.2%, 1.3%, and 0.1% of the total GSL content (Fig. 2). The GBR content was significantly higher than in the other groups, and the mean antioxidant activity was the highest. In color group 3, the mean GRH, GRE, GBR, GER, and GBE contents were, respectively, 6,807.1, 2,560.2, 253.9, 219.7, and 24 ㎍/g DW, comprising 69%, 26%, 2.6%, 2.2%, and 0.2% of the total GSL content. The individual GSL contents were significantly higher than in the other groups, but unexpectedly, the mean antioxidant activity (DPPH free-radical scavenging activity) was not high.

In color group 4, the mean GRH, GRE, GBR, GER, and GBE contents were, respectively, 5,361.1, 1,732.7, 95.2, 172, and 11.4 ㎍/g DW, comprising 72.9%, 23.6%, 1.1%, 2.3%, and 0.2% of the total GSL content. In color group 5, the mean GRH, GRE, GBR, GER, and GBE contents were, respectively, 6,041.3, 1,440.4, 95.2, 174.8, and 12.6 ㎍/g DW, comprising 77.8%, 18.6%, 1.2%, 2.3%, and 0.2% of the total GSL content (7,764.3 ㎍/g DW). Radishes belong to this group are known as kimchi radishes and are particularly preferred in Korea.

Discussion

We found that various phenotypic traits were highly correlated with each other. In cases where desirable and undesirable traits are highly correlated, breeding programs employ selection processes to uncouple the correlations. According to Jatoi et al. (2011), Twe was highly correlated with Lwi (r = 0.70) and RL (r = 0.71) in their radish samples. In this study, we observed a significant correlation between Twe and LL (r = 0.65), as did Jatoi et al. (2011). Color is an important external characteristic used to evaluate radish quality. Customers in Korea prefer white radishes with green shoulders. This type of radish has a sweet taste and crispy texture, and is popularly used to make kimchi, a traditional Korean side dish, along with soups and various other side dishes. Consumers often modify their dietary habits to improve health. This could explain the recent increase in popularity of food products derived from Brassica vegetables, and the development of experimental products such as broccoli puree with lactic acid (Cai et al., 2019) and muffins enriched with dietary fiber from kimchi (Heo et al., 2019). Brassica plants contain GSLs that can be degraded by intestinal microorganisms to produce bioactive metabolites such as isothiocyanates, which have anti-cancer and other biological properties (Aires et al., 2009). In this study, five GSLs, four aliphatic GSLs (GER, GRH, GRE, and GBE) and one indole GSL (GBR) were screened and quantified in 110 radish germplasms. Three aliphatic GSLs (GRH, GER, and GBE) were significantly correlated with one another but not with GBE or the indole GSL, GBR. This could be due to differences in biosynthetic pathways and precursors, with GRH, GER, and GBE sharing a similar 4C pathway, whereas GBE is derived from a 5C pathway. GBR, the indole GSL, has a different amino-acid precursor, tryptophan.

The GSL contents in radish were found to be correlated with some phenotypic traits. The total GSL content was significantly correlated with LL but not with RL. A similar observation was reported for kimchi cabbage by Jeon et al. (2018) and Kakizaki et al. (2017), who studied the synthesis and movement of GSL (Jeon et al., 2018; Kakizaki et al., 2017). Yi et al. (2016) reported no strong correlations among root shape, pithiness, sweetness, peel color, length, and GSL content (Yi et al., 2016). Root phenotypic characters such as color, shape, and length were not strongly associated with the GSL profile of the radish germplasms in this study, implying that the root phenotype does not reflect GSL contents. However, based on this finding, it may be possible to develop radish varieties of various phenotypes with high GSL contents.

According to our PCA, GSL contents were not strongly correlated with DPPH activity. Raphasatin, a degradation product of GRH, was reported to more potently induce detoxification enzymes than other degradation products (Scholl et al., 2011; Suzuki et al., 2016). A more complete understanding of the overall antioxidant effect could be achieved by measuring the antioxidant activities of isothiocyanates such as raphasatin. The germplasms in Group III in the PCA plot in Fig. 1 produce small red radishes with high DPPH free-radical scavenging activities. To determine whether the antioxidant effect is influenced by the root size or red pigment, small non-red radish germplasms can be analyzed. Red radishes contain higher levels of high anthocyanins and other phenolic compounds than non-pigmented radishes (Singh et al., 2017). Hence, they can be used to prepare healthful, nutrient-dense dishes and nutraceutical formulations.

In this study, we assessed various phenotypic traits, DPPH free-radical scavenging activity, and the contents of five GSLs in radish germplasms. The results regarding GSL levels in radishes, and their relationships with leaf and root characteristics, could be used as baseline data by breeders and nutraceutical companies. Moreover, the biochemical and phenotypic information provided by this study may encourage consumers to diversify their eating habits.

Appendix

Appendix 1.

Qualitative phenotype characters of 110 germplasms and 10 Korean cultivars

No. IT No. Root peel color Root shoulder color Root fresh color Root shape Root position in soil
1 32729 White Green White N-rectangle Half B
2 100590 White Green White Rectangle Half B
3 100649 White Green White N-rectangle Half B
4 100678 White Green White Rectangle Mostly B
5 100684 White Green White Almond Mostly B
6 100689 White Green White Egg Half B
7 100691 White Green White Rectangle Mostly B
8 100695 White Green White Rectangle Half B
9 102376 White Green White N-rectangle Mostly B
10 102378 White Green White N-rectangle Half B
11 102395 White Green White N-rectangle Half B
12 102560 Red Red White Egg Half B
13 103802 White Green White Rectangle Mostly B
14 103811 White Green White Oval Mostly B
15 104055 White Green White W-rectangle Mostly B
16 112253 White White White N-rectangle Mostly B
17 112255 White White White N-rectangle Mostly B
18 112257 White White White N-rectangle Mostly B
19 112258 White White White N-rectangle Mostly B
20 119000 White Green White Rectangle Mostly B
21 136485 White White White N-rectangle Mostly B
22 136498 Red Red White Spherical Mostly A
23 166993 White White White Rectangle Mostly B
24 166995 White White White N-rectangle Half B
25 166997 White White White N-rectangle Mostly B
26 185738 White Green White Egg Mostly B
27 188102 Bronze-green Bronze-green Green W-rectangle Mostly A
28 203316 Bronze-green Bronze-green Green W-Oval Mostly A
29 203531 White Green White Rectangle Mostly B
30 204160 White Green White Rectangle Mostly B
31 208400 Red Red White Egg Mostly A
32 209937 Bronze-green Bronze-green Green Egg Mostly A
33 209974 White White White N-rectangle Half B
34 210203 White White White N-rectangle Mostly B
35 213153 White Green White Egg Mostly B
36 215011 White Green White Gourd Mostly B
37 215079 White White White N-rectangle Half B
38 218925 White Green White Egg Mostly B
39 220675 Bronze-green Bronze-green Green Egg Mostly A
40 221952 Bronze-green Bronze-green Green Rectangle Mostly A
41 221955 White White White Almond Mostly B
42 221956 White White White Almond Mostly B
43 221958 White White White Almond Half B
44 221959 White White White Rectangle Half B
45 223576 Bronze-green Bronze-green Green W-rectangle Above
46 228857 Bronze-green Bronze-green Green Egg Above
47 228870 Bronze-green Bronze-green Green Spherical Above
48 250738 White White White N-rectangle Mostly B
49 250765 White White White N-rectangle Mostly B
50 250775 Bronze-green Bronze-green Green Spherical Above
51 250777 Bronze-green Bronze-green Green Egg Above
52 250788 White White White N-rectangle Mostly B
53 250790 White White White W-rectangle Mostly B
54 250792 Bronze-green Bronze-green Green Rectangle Mostly A
55 250794 Bronze-green Bronze-green Green Rectangle Mostly A
56 261944 Red Red White Spherical Half B
57 261947 White White White N-rectangle Half B
58 261953 White White White Spherical Half B
59 261954 White Green White N-rectangle Mostly B
60 261955 Bronze-green Bronze-green Green N-rectangle Mostly A
61 261967 White White White N-rectangle Mostly B
62 261978 Red Red White Spherical Half B
63 261989 White White White N-rectangle Mostly B
64 261995 White White White N-rectangle Half B
65 262006 White White White Egg Mostly B
66 262018 White White White Rectangle Mostly B
67 262022 White White White N-rectangle Mostly B
68 262023 White White White W-rectangle Half B
69 262031 Red Red White Spherical Half B
70 262032 Bronze-green Bronze-green Green W-rectangle Above
71 262036 White Green Red Spherical Half B
72 262037 White White White N-rectangle Mostly B
73 262044 White White White Almond Half B
74 262049 White Green Red Spherical Half B
75 262050 Red Red White W-Oval Half B
76 262057 White Green White Oval Mostly B
77 262070 Red Red White W-Oval Half B
78 262075 White White White Spherical Half B
79 262076 White White White Spherical Mostly B
80 264178 White Green Red Spherical Half B
81 264180 White White White Spherical Mostly B
82 276165 White White White N-rectangle Mostly A
83 278269 White White White W-rectangle Mostly B
84 278682 White Green Red W-rectangle Half B
85 278683 Bronze-green Bronze-green Green N-rectangle Mostly A
86 278684 White White White N-rectangle Mostly A
87 278685 White White White N-rectangle Mostly B
88 278727 Red Red White Spherical Mostly A
89 283305 White White White Spherical Mostly B
90 283312 White Green White N-rectangle Mostly B
91 283317 Red Red White Spherical Half B
92 289244 White Green Red Spherical Half B
93 291383 Red Red White Egg Half B
94 291423 White Green White Oval Mostly B
95 291541 White White White Rectangle Mostly B
96 293006 White White White Spherical Mostly B
97 293008 White Green White N-rectangle Mostly B
98 293028 White Green White Egg Mostly B
99 293085 White Green White Oval Mostly B
100 297120 White Green Red Spherical Half B
101 297172 Red Red White Spherical Mostly A
102 297174 White White White Rectangle Mostly B
103 299326 Bronze-green Bronze-green Green N-rectangle Mostly A
104 299453 Bronze-green Bronze-green Green N-rectangle Mostly A
105 305085 White Green White Rectangle Half B
106 305381 Bronze Bronze-green Green Rectangle Mostly A
107 306869 White White White W-Oval Mostly B
108 308359 Red Red White Spherical Half B
109 308367 Bronze-green Bronze-green Green Rectangle Mostly A
110 308418 White White White N-rectangle Mostly B
Con1 Gwailmu White Green Red W-rectangle Half B
Con2 Meosjinmaskkalmu White Green White Oval Half B
Con3 Taecheong White Green White Oval Mostly A
Con4 Cheong-unmu White Green White Oval Half B
Con5 Chorongmu White Green White Gourd Mostly B
Con6 Mansa-hyeongtongmu White Green White Oval Half B
Con7 Togwanggoldeumu White Green White Egg Mostly B
Con8 Baeksinaltari White Green White Gourd Mostly B
Con9 Syupeogiljomu White Green White Oval Half B
Con10 Seohogoldeumu White Green White Oval Half B

In root position in soil, Above: above soil line, Mostly A: mostly above soil line, Half B: half buried, Mostly B: mostly buried.

Appendix 2.

Quantitative phenotype characters of 110 germplasms and 10 Korean cultivars

No. IT No. Total
weight
Leaf
weight
Root
weight
Weight
ratio
(Top/Root)
Root
length
(cm)
Root
width
(cm)
Root
ratio
(Length/
Width)
Leaf
length
Leaf
width
Leaf
ratio
(Length/
Width)
Leaf
number
1 32729 2140.0 451.7 1688.3 0.27 36.3 8.4 4.30 50.1 17.1 2.9 25.3
2 100590 2268.3 913.3 1355.0 0.67 24.1 9.8 2.50 56.9 17.0 3.4 35.7
3 100649 1921.7 546.7 1375.0 0.40 26.0 9.0 2.90 48.8 15.3 3.2 40.0
4 100678 2388.4 621.7 1766.7 0.35 26.0 10.3 2.50 53.8 17.8 3.0 32.0
5 100684 2381.7 816.7 1565.0 0.52 26.7 13.8 1.90 50.2 18.5 2.7 30.3
6 100689 1550.0 258.3 1291.7 0.20 21.0 10.4 2.00 35.3 14.3 2.5 18.3
7 100691 2360.0 550.0 1810.0 0.30 22.0 11.1 2.00 54.8 19.3 2.8 37.3
8 100695 2243.3 745.0 1498.3 0.50 24.8 10.2 2.40 47.7 15.3 3.1 42.0
9 102376 2203.3 801.7 1401.7 0.57 31.3 8.8 3.60 51.5 16.5 3.1 38.0
10 102378 2978.4 856.7 2121.7 0.40 41.0 9.2 4.50 50.3 16.7 3.0 43.3
11 102395 2268.3 988.3 1280.0 0.77 31.7 8.3 3.80 50.1 22.3 2.3 27.3
12 102560 1641.7 586.7 1055.0 0.56 21.7 9.1 2.40 46.8 19.6 2.4 14.0
13 103802 2288.3 768.3 1520.0 0.51 19.0 11.3 1.70 54.0 19.8 2.7 29.3
14 103811 2091.7 823.3 1268.3 0.65 19.8 10.7 1.90 55.0 20.2 2.7 27.0
15 104055 1324.3 301.0 1023.3 0.29 17.3 9.7 1.80 48.2 17.7 2.7 25.3
16 112253 1658.3 1013.3 645.0 1.57 28.2 6.3 4.50 46.3 15.3 3.0 47.3
17 112255 1686.7 706.7 980.0 0.72 36.3 6.6 5.50 46.8 13.5 3.5 47.0
18 112257 2996.6 1833.3 1163.3 1.58 40.7 7.2 5.70 57.8 23.3 2.5 47.0
19 112258 3308.3 390.0 2918.3 0.13 48.0 12.8 3.80 44.9 15.3 2.9 50.0
20 119000 1910.3 643.7 1266.7 0.51 22.5 10.1 2.20 50.0 12.2 4.1 28.7
21 136485 1681.7 951.7 730.0 1.30 28.7 6.2 4.60 49.5 17.8 2.8 41.3
22 136498 45.4 0.4 45.0 0.01 2.5 2.1 1.20 19.6 9.2 2.1 10.3
23 166993 2211.6 758.3 1453.3 0.52 35.7 8.1 4.40 53.2 19.7 2.7 27.3
24 166995 1801.6 273.3 1528.3 0.18 39.0 8.2 4.80 36.2 13.1 2.8 35.7
25 166997 2253.3 665.0 1588.3 0.42 36.7 8.4 4.40 47.2 19.0 2.5 40.7
26 185738 1186.6 328.3 858.3 0.38 19.7 9.5 2.10 41.3 18.7 2.2 16.3
27 188102 2045.0 515.0 1530.0 0.34 23.7 10.5 2.30 45.9 22.7 2.0 18.3
28 203316 1865.0 726.7 1138.3 0.64 9.3 13.5 0.70 45.3 19.3 2.4 18.0
29 203531 2161.7 836.7 1325.0 0.63 27.7 8.5 3.30 52.3 13.5 3.9 30.7
30 204160 1756.6 583.3 1173.3 0.50 20.7 9.5 2.20 49.2 17.3 2.8 23.0
31 208400 228.3 60.3 168.0 0.36 8.5 7.0 1.20 26.8 13.2 2.0 10.7
32 209937 1441.7 361.7 1080.0 0.33 13.0 12.3 1.10 44.5 15.3 2.9 12.3
33 209974 1420.0 220.0 1200.0 0.18 36.2 8.9 4.10 27.3 12.0 2.3 35.0
34 210203 2163.4 546.7 1616.7 0.34 39.7 8.0 5.00 39.3 15.5 2.5 37.7
35 213153 1838.4 546.7 1291.7 0.42 18.3 11.8 1.60 45.0 15.4 2.9 31.3
36 215011 2176.7 786.7 1390.0 0.57 19.8 10.8 1.80 49.0 16.8 2.9 24.7
37 215079 2455.0 938.3 1516.7 0.62 39.7 8.4 4.70 46.8 17.5 2.7 52.0
38 218925 1786.7 370.0 1416.7 0.26 22.8 9.8 2.30 47.5 14.2 3.4 20.0
39 220675 2018.3 473.3 1545.0 0.31 17.2 11.3 1.50 53.9 18.1 3.0 16.7
40 221952 991.7 271.7 720.0 0.38 17.8 7.6 2.30 40.1 11.6 3.5 16.3
41 221955 2836.7 761.7 2075.0 0.37 34.3 10.5 3.30 54.8 20.8 2.6 22.7
42 221956 2688.4 656.7 2031.7 0.32 32.7 41.8 0.80 54.3 19.2 2.8 18.3
43 221958 1490.0 186.7 1303.3 0.14 43.2 8.5 5.10 27 11.3 2.4 27.3
44 221959 2146.7 455.0 1691.7 0.27 31.0 9.0 3.40 42.8 13.8 3.1 25.0
45 223576 1293.3 253.3 1040.0 0.24 18.7 9.4 2.00 41.2 15.8 2.6 16.5
46 228857 1366.7 380.0 986.7 0.39 16.2 9.8 1.70 45.9 18.0 2.6 16.3
47 228870 1525.0 373.3 1151.7 0.32 13.5 11.6 1.20 48.3 17.3 2.8 15.3
48 250738 2383.3 843.3 1540.0 0.55 45.3 7.5 6.00 62.0 17.9 3.5 40.0
49 250765 2616.4 869.7 1746.7 0.50 45.4 7.3 6.20 46.5 17.8 2.6 40.3
50 250775 1475.0 411.7 1063.3 0.39 11.8 11.9 1.00 48.9 22.3 2.2 14.0
51 250777 1605.0 273.3 1331.7 0.21 16.2 12.4 1.30 46.2 18.3 2.5 12.7
52 250788 3073.3 788.3 2285.0 0.34 36.0 10.5 3.40 54.7 21.6 2.5 26.0
53 250790 2678.3 660.0 2018.3 0.33 32.3 10.6 3.00 49.8 16.4 3.0 19.0
54 250792 1481.7 340.0 1141.7 0.30 24.3 8.3 2.90 44.7 17.1 2.6 15.0
55 250794 1796.6 393.3 1403.3 0.28 25.0 9.1 2.70 44.9 19.9 2.3 17.0
56 261944 2176.6 698.3 1478.3 0.47 12.4 13.6 0.90 52.9 20.9 2.5 25.3
57 261947 2280.0 608.3 1671.7 0.36 33.5 9.1 3.70 51.7 18.7 2.8 19.7
58 261953 1295.0 341.7 953.3 0.36 12.7 12.0 1.10 42.3 14.5 2.9 28.0
59 261954 2276.7 1021.7 1255.0 0.81 32.4 6.9 4.70 53.5 21.8 2.5 40.7
60 261955 1645.0 418.3 1226.7 0.34 29.4 7.8 3.80 47.1 25.8 1.8 13.0
61 261967 2566.7 646.7 1920.0 0.34 32.8 9.5 3.50 58.6 18.1 3.2 16.7
62 261978 1888.3 700.0 1188.3 0.59 12.7 12.3 1.00 53.7 18.9 2.8 24.7
63 261989 2670.0 1031.7 1638.3 0.63 41.5 7.8 5.30 42.6 15.3 2.8 42.0
64 261995 1440.0 176.7 1263.3 0.14 39.1 8.1 4.80 26.2 10.3 2.5 26.7
65 262006 1988.3 688.3 1300.0 0.53 25.0 10.1 2.50 54.4 17.0 3.2 23.0
66 262018 1953.3 865.0 1088.3 0.79 25.8 8.5 3.00 51.3 16.5 3.1 31.3
67 262022 2750.0 608.3 2141.7 0.28 36.0 10.6 3.40 44.2 21.6 2.1 16.7
68 262023 1336.7 365.0 971.7 0.38 18.7 9.4 2.00 44.4 10.8 4.1 29.0
69 262031 743.3 270.0 473.3 0.57 10.0 9.8 1.00 46.6 15.5 3.0 22.7
70 262032 1571.6 243.3 1328.3 0.18 19.7 9.9 2.00 44.5 21.9 2.0 11.7
71 262036 1195.0 373.3 821.7 0.45 11.0 11.5 1.00 41.6 17.5 2.4 21.7
72 262037 2120.0 865.0 1255.0 0.69 33.8 7.5 4.50 48.6 15.8 3.1 44.0
73 262044 1560.0 405.0 1155.0 0.35 23.0 9.7 2.40 55.5 16.1 3.5 14.3
74 262049 1370.0 463.3 906.7 0.51 11.7 11.5 1.00 47.4 19.7 2.4 17.0
75 262050 1598.4 431.7 1166.7 0.37 10.8 12.9 0.80 47.5 18.1 2.6 19.0
76 262057 2025.0 758.3 1266.7 0.60 20.7 9.9 2.10 59.8 18.5 3.2 25.3
77 262070 1838.4 396.7 1441.7 0.28 10.2 13.6 0.80 52.6 21.2 2.5 17.3
78 262075 1720.0 416.7 1303.3 0.32 15.7 13.0 1.20 42.6 14.0 3.0 26.7
79 262076 1936.6 428.3 1508.3 0.28 13.1 14.1 0.90 44.3 13.8 3.2 28.3
80 264178 1596.6 493.3 1103.3 0.45 12.3 12.3 1.00 48.2 20.1 2.4 21.0
81 264180 2265.0 643.3 1621.7 0.40 12.7 15.0 0.80 50.2 13.2 3.8 30.7
82 276165 1768.3 300.0 1468.3 0.20 37.5 9.0 4.20 36.1 12.0 3.0 29.3
83 278269 1200.0 265.0 935.0 0.28 20.4 9.1 2.20 37.6 10.2 3.7 25.7
84 278682 1496.7 426.7 1070.0 0.40 12.8 10.8 1.20 44.3 15.9 2.8 20.3
85 278683 1235.0 226.7 1008.3 0.22 28.0 7.2 3.90 38.9 18.1 2.2 11.0
86 278684 1373.3 160.0 1213.3 0.13 38.2 8.2 4.70 27.1 10.4 2.6 24.3
87 278685 1621.7 326.7 1295.0 0.25 29.5 8.7 3.40 42.2 15.1 2.8 18.3
88 278727 155.0 30.0 125.0 0.24 6.8 6.4 1.10 21.1 9.3 2.3 11.0
89 283305 2213.3 903.3 1310.0 0.69 14.7 11.8 1.20 49.7 16.8 3.0 59.0
90 283312 1380.0 471.7 908.3 0.52 26.0 7.4 3.50 40.4 14.4 2.8 30.3
91 283317 1990.0 641.7 1348.3 0.48 13.7 13.4 1.00 40.2 18.7 2.2 22.7
92 289244 1271.7 461.7 810.0 0.57 10.7 10.7 1.00 46.5 16.7 2.8 20.0
93 291383 195.0 39.0 156.0 0.25 9.5 6.0 1.60 22.7 12.4 1.8 10.7
94 291423 3278.3 855.0 2423.3 0.35 21.5 14.5 1.50 52.6 17.6 3.0 40.3
95 291541 1645.0 541.7 1103.3 0.49 34.3 6.9 5.00 38.7 15.6 2.5 43.7
96 293006 1875.0 583.3 1291.7 0.45 11.0 13.3 0.80 40.4 14.9 2.7 48.0
97 293008 2195.0 616.7 1578.3 0.39 39.3 8.1 4.90 48.3 15.9 3.0 33.0
98 293028 2238.3 820.0 1418.3 0.58 16.2 11.8 1.40 50.3 18.0 2.8 30.3
99 293085 2271.7 901.7 1370.0 0.66 18.0 12.9 1.40 53.3 19.2 2.8 33.0
100 297120 1425.0 470.0 955.0 0.49 9.5 12.3 0.80 43.7 17.8 2.5 21.0
101 297172 68.3 13.0 55.3 0.24 5.5 4.7 1.20 14.2 8.4 1.7 8.7
102 297174 3420.0 583.3 2836.7 0.21 42.0 10.9 3.90 45.3 18.6 2.4 30.0
103 299326 1430.0 336.7 1093.3 0.31 33.0 7.1 4.60 61.5 19.2 3.2 13.0
104 299453 1226.7 261.7 965.0 0.27 32.2 6.3 5.10 40.2 18.6 2.2 12.3
105 305085 1513.0 668.0 845.0 0.79 15.8 8.5 1.90 57.7 18.9 3.1 32.3
106 305381 1693.4 441.7 1251.7 0.35 23.3 8.8 2.60 44.7 20.0 2.2 17.7
107 306869 1260.3 515.3 745.0 0.69 8.0 11.7 0.70 44.4 12.8 3.5 38.7
108 308359 1586.7 376.7 1210.0 0.31 11.7 12.4 0.90 43.7 16.8 2.6 19.0
109 308367 1208.4 286.7 921.7 0.31 23.7 7.7 3.10 39.8 16.0 2.5 18.0
110 308418 1383.4 166.7 1216.7 0.14 36.2 7.9 4.60 25.3 9.6 2.6 28.0
Con1 Gwailmu 1071.7 245.0 826.7 0.30 12.0 10.5 1.14 32.3 15.3 2.1 22.3
Con2 Meosjinmaskkalmu 2008.3 233.3 1775.0 0.13 21.2 11.4 1.86 35.6 14.1 2.5 29.7
Con3 Taecheong 2636.7 473.3 2163.3 0.22 24.2 11.8 2.05 41.5 17.3 2.4 28.3
Con4 Cheong-unmu 2380.0 340.0 2040.0 0.17 24.6 12.4 1.98 42.1 17.6 2.4 20.0
Con5 Chorongmu 2083.3 363.3 1720.0 0.21 19.2 12.0 1.60 45.6 16.4 2.8 26.7
Con6 Mansa-hyeongtongmu 2371.7 410.0 1961.7 0.21 24.2 11.7 2.07 36.2 11.8 3.1 33.0
Con7 Togwanggoldeumu 2113.3 165.0 1948.3 0.08 19.5 12.4 1.57 35.9 17.9 2.0 20.3
Con8 Baeksinaltari 723.3 135.0 588.3 0.23 12.3 11.7 1.05 38.1 12.3 3.1 19.0
Con9 Syupeogiljomu 2721.7 575.0 2146.7 0.27 23.2 12.0 1.93 48.3 18.9 2.5 27.7
Con10 Seohogoldeumu 2776.7 413.3 2363.3 0.17 25.8 12.6 2.05 43.1 17.3 2.5 23.7
Appendix 3.

Glucosinolate contents and DPPH activity of 110 germplasms and 10 Korean cultivars

No. IT No. Glucoraphasatin
(Average
± SDz)
Glucoraphenin
(Average
± SDz)
Glucobrassicin
(Average
± SDz)
Glucoerucin
(Average
± SDz)
Glucoberteroin
(Average
± SDz)
Total
glucosinolate
(Average
± SDz)
DPPH
activity
(%)
1 32729 11179.03
± 925.59
2656.67
± 263.93
124.37
± 11.06
319.76
± 34.11
24.41
± 1.81
14304.24
± 1234.00
22.29
± 0.50
2 100590 10939.58
± 1419.28
1778.49
± 326.62
134.18
± 19.91
360.22
± 55.2
35.83
± 1.74
13248.31
± 1814.64
27.60
± 1.46
3 100649 2793.50
± 266.26
546.68
± 66.83
28.93
± 3.83
27.23
± 2.01
4.36
± 0.69
3400.70
± 338.45
26.02
± 0.90
4 100678 984.87
± 121.39
472.46
± 58.10
8.27
± 1.37
9.50
± 1.06
0.66
± 0.32
1475.75
± 181.93
19.08
± 1.52
5 100684 5945.12
± 390.38
1713.83
± 149.23
220.70
± 19.95
133.37
± 13.98
7.90
± 0.49
8020.92
± 571.75
30.90
± 1.76
6 100689 975.52
± 126.22
747.44
± 91.26
9.40
± 1.31
13.62
± 1.78
1.40
± 0.52
1747.39
± 220.09
31.48
± 0.68
7 100691 6291.06
± 689.13
1917.39
± 198.31
39.06
± 5.74
102.17
± 11.39
7.99
± 1.19
8357.66
± 900.7
31.26
± 0.79
8 100695 8476.9
± 735.11
2411.44
± 167.18
288.21
± 37.26
349.47
± 23.76
34.62
± 2.69
11560.65
± 964.07
20.80
± 0.49
9 102376 11261.78
± 1145.72
1502.84
± 220.68
76.77
± 8.16
324.42
± 40.68
14.46
± 1.53
13180.27
± 1411.31
15.70
± 1.29
10 102378 11695.28
± 1055.43
2455.14
± 398.31
312.01
± 23.76
291.55
± 36.15
20.95
± 1.55
14774.93
± 1514.06
14.70
± 2.24
11 102395 5475.85
± 383.85
1328.9
± 162.74
96.22
± 12.31
124.27
± 7.75
7.59
± 1.52
7032.84
± 564.16
21.60
± 0.21
12 102560 9565.98
± 355.89
2899.40
± 124.44
184.77
± 5.41
378.23
± 9.46
15.62
± 0.28
13043.99
± 492.01
16.02
± 2.06
13 103802 2815.52
± 219.04
920.06
± 104.04
94.09
± 10.92
36.37
± 2.68
4.59
± 0.54
3870.64
± 336.22
19.18
± 0.42
14 103811 210.71
± 18.73
57.83
± 9.42
0.87
± 0.24
4.72
± 0.09
0.24
± 0.15
274.37
± 23.51
10.43
± 2.22
15 104055 2462.68
± 284.12
1045.55
± 115.08
55.75
± 7.52
36.83
± 4.43
3.47
± 0.86
3604.28
± 411.71
18.29
± 2.17
16 112253 252.61
± 26.96
43.70
± 5.47
3.93
± 0.31
3.70
± 0.65
0.18
± 0.09
304.12
± 32.98
12.47
± 0.98
17 112255 7013.84
± 811.76
1871.35
± 326.49
122.35
± 12.8
98.84
± 13.09
11.33
± 0.69
9117.71
± 1161.6
16.09
± 2.80
18 112257 9441.1
± 750.17
936.32
± 120.22
82.20
± 6.39
215.41
± 21.63
11.19
± 0.72
10686.21
± 897.43
19.89
± 2.80
19 112258 8996.09
± 747.33
1596.7
± 212.78
33.80
± 2.64
445.24
± 43.83
20.56
± 1.20
11092.39
± 1006.74
18.59
± 2.03
20 119000 9305.38
± 986.46
2231.75
± 405.44
60.17
± 8.26
284.83
± 45.92
19.36
± 3.54
11901.48
± 1449.54
16.47
± 1.35
21 136485 8551.15
± 740.75
735.01
± 75.20
43.17
± 5.30
247.89
± 23.55
23.8
± 1.33
9601.02
± 830.78
32.49
± 2.57
22 136498 3116.76
± 306.78
901.86
± 105.92
29.20
± 2.68
48.98
± 5.56
2.89
± 0.17
4099.69
± 417.29
52.69
± 0.59
23 166993 508.27
± 41.06
379.03
± 34.81
4.71
± 0.18
6.54
± 0.97
0.38
± 0.25
898.94
± 77.13
18.29
± 0.20
24 166995 5828.08
± 876.35
1862.04
± 430.71
225.72
± 32.85
191.62
± 39.33
4.67
± 0.37
8112.13
± 1377.45
28.77
± 1.54
25 166997 423.77
± 49.42
207.6
± 27.75
2.08
± 0.33
6.37
± 0.39
0.29
± 0.26
640.11
± 77.01
21.26
± 0.30
26 185738 691.98
± 50.89
316.58
± 44.00
8.12
± 0.19
16.64
± 2.18
0.49
± 0.29
1033.8
± 96.62
18.72
± 1.10
27 188102 1615.38
± 212.87
924.99
± 132.93
18.92
± 2.07
23.6
± 4.24
2.21
± 0.28
2585.11
± 349.14
16.35
± 1.66
28 203316 3715.43
± 452.50
1964.29
± 284.38
158.21
± 17.09
74
± 12.10
9.11
± 1.91
5921.04
± 766.50
20.27
± 1.55
29 203531 3095.72
± 309.97
960.01
± 100.11
6.43
± 0.65
51.49
± 7.02
4.38
± 0.48
4118.03
± 418.05
16.3
± 1.14
30 204160 4668.71
± 590.22
1118.75
± 181.58
59.03
± 8.37
98.51
± 14.91
9.54
± 1.09
5954.54
± 795
32.84
± 0.63
31 208400 814.68
± 102.08
499.81
± 132.81
5.28
± 0.80
13.73
± 1.72
0.49
± 0.52
1334
± 237.12
59.81
± 0.69
32 209937 3424.68
± 322.98
1808.17
± 184.18
88.7
± 8.17
62.04
± 7.73
8.31
± 1.33
5391.9
± 520.24
23.78
± 0.64
33 209974 5093.86
± 688.86
1111.8
± 163.98
90.38
± 12.64
172.77
± 33.28
5.36
± 0.62
6474.17
± 890.91
27.58
± 1.73
34 210203 4050.15
± 447.00
814.92
± 85.05
8.69
± 1.15
89.41
± 9.81
13.08
± 1.31
4976.25
± 537.67
24.90
± 0.34
35 213153 662.76
± 62.28
510.75
± 42.22
1.56
± 0.04
12.63
± 1.68
0.41
± 0.11
1188.11
± 105.84
18.81
± 0.51
36 215011 12921.97
± 1252.18
2527.07
± 295.34
134.99
± 15.18
440.03
± 37.63
49.69
± 5.37
16073.75
± 1549.92
28.79
± 2.41
37 215079 9803.19
± 806.83
1700.19
± 165.18
26.87
± 1.41
348.51
± 36.71
19.78
± 1.74
11898.55
± 1004.35
12.85
± 1.84
38 218925 11321.86
± 1208.50
2160.83
± 292.20
165.04
± 11.76
512.00
± 66.73
18.62
± 3.07
14178.35
± 1579.41
26.19
± 0.88
39 220675 7562.46
± 1027.86
3389.28
± 570.44
296.17
± 45.93
199.11
± 36.77
23.76
± 2.53
11470.77
± 1667.16
19.78
± 1.69
40 221952 8634.13
± 975.11
3140.49
± 364.04
338.87
± 36.89
305.60
± 30.6
43.56
± 3.06
12462.65
± 1402.28
30.83
± 2.51
41 221955 7544.73
± 930.51
3883.83
± 522.85
28.75
± 6.21
249.00
± 28.87
16.74
± 1.17
11723.95
± 1461.62
33.26
± 1.74
42 221956 7179.87
± 775.79
2988.78
± 407.06
84.45
± 5.87
227.86
± 31.48
17.77
± 0.82
10498.74
± 1200.09
21.33
± 1.51
43 221958 325.33
± 36.35
174.68
± 19.07
5.33
± 0.55
6.82
± 1.01
0.15
± 0.16
512.31
± 56.99
18.79
± 0.36
44 221959 1407.71
± 166.67
616.06
± 115.42
23.68
± 2.93
27.61
± 2.34
1.21
± 0.43
2076.27
± 259.33
34.57
± 0.56
45 223576 9678.29
± 1323.37
4284.93
± 551.12
224.54
± 25.15
319.74
± 63.01
27.68
± 6.77
14535.19
± 1926.59
19.13
± 1.24
46 228857 8046.57
± 861.63
3748.14
± 391.37
203.22
± 31.25
291.04
± 31.17
29.59
± 3.50
12318.56
± 1309.22
30.39
± 1.30
47 228870 11638.83
± 1215.04
5105.15
± 531.94
631.39
± 129.13
371.71
± 66.63
42.26
± 5.75
17789.35
± 1943.58
15.50
± 1.49
48 250738 10414.1
± 1215.68
1451.88
± 179.06
113.52
± 13.35
319.07
± 56.43
23.71
± 3.37
12322.28
± 1465.38
20.90
± 2.22
49 250765 5443.16
± 507.96
1471.51
± 169.37
33.07
± 3.07
158.79
± 22.78
6.64
± 0.84
7113.17
± 702.02
17.24
± 2.05
50 250775 6514.06
± 588.64
2636.95
± 282.67
76.41
± 13.88
187.94
± 17.38
20.89
± 1.41
9436.24
± 902.71
24.64
± 1.09
51 250777 1161.23
± 62.82
791.86
± 133.05
35.20
± 0.57
20.95
± 0.95
1.62
± 0.13
2010.85
± 190.33
17.84
± 2.31
52 250788 5719.88
± 455.08
3293.35
± 115.39
99.63
± 6.72
174.70
± 22.87
9.98
± 0.35
9297.54
± 599.10
23.80
± 0.88
53 250790 7527.83
± 836.51
4421.21
± 418.65
129.48
± 12.02
192.34
± 35.84
13.09
± 2.04
12283.96
± 1257.89
40.63
± 12.15
54 250792 6315.22
± 618.27
1035.81
± 107.50
246.75
± 21.10
138.07
± 20.15
13.6
± 0.83
7749.45
± 759.18
16.00
± 3.17
55 250794 7707.88
± 564.45
2828.78
± 381.80
186.71
± 24.00
214.64
± 23.35
23.55
± 1.12
10961.55
± 982.87
22.08
± 2.48
56 261944 4715.3
± 607.44
496.67
± 64.25
119.13
± 15.15
100.22
± 11.55
5.38
± 0.39
5436.7
± 697.13
28.00
± 0.97
57 261947 8035.35
± 729.44
3329.76
± 180.91
70.63
± 8.33
263.42
± 41.36
13.94
± 3.22
11713.1
± 937.09
27.53
± 3.00
58 261953 4415.55
± 456.00
1237.84
± 144.58
73.36
± 9.98
79.53
± 7.91
7.44
± 0.99
5813.72
± 613.45
32.54
± 1.56
59 261954 6710.18
± 713.28
2105.59
± 250.08
64.73
± 12.06
126.48
± 13.04
6.60
± 0.21
9013.58
± 987.87
14.61
± 1.67
60 261955 7185.08
± 813.15
1960.97
± 255.23
196.25
± 28.85
187.04
± 18.21
17.68
± 1.06
9547.02
± 1115.79
21.06
± 0.80
61 261967 8442.83
± 1006.26
3438.58
± 446.30
124.64
± 18.12
262.36
± 25.49
23.77
± 1.89
12292.18
± 1482.31
21.88
± 1.94
62 261978 974.68
± 48.05
302.64
± 22.48
7.83
± 0.38
13.93
± 0.93
0.79
± 0.32
1299.86
± 68.28
24.38
± 3.71
63 261989 10760.66
± 977.97
3121.63
± 339.26
26.72
± 2.51
520.92
± 77.72
32.17
± 1.59
14462.1
± 1329.74
20.40
± 2.37
64 261995 2167.39
± 226.85
1547.31
± 160.31
2.98
± 0.19
40.01
± 5.13
2.80
± 0.31
3760.5
± 370.32
18.38
± 3.10
65 262006 423.06
± 22.30
248.22
± 15.75
4.21
± 0.13
7.90
± 0.20
0.26
± 0.09
683.65
± 30.19
21.39
± 1.64
66 262018 147.42
± 6.48
29.23
± 1.59
0.65
± 0.07
2.58
± 0.18
0.05
± 0.06
179.92
± 7.33
24.59
± 2.02
67 262022 8475.89
± 920.77
4146.82
± 408.09
38.22
± 2.66
310.78
± 43.94
28.01
± 2.13
12999.72
± 1372.38
24.59
± 2.17
68 262023 184.02
± 22.47
59.04
± 8.60
1.36
± 0.13
2.40
± 0.09
0.00
± 0.00
246.82
± 31.22
27.57
± 2.23
69 262031 1082.49
± 98.07
778.41
± 50.81
10.68
± 0.77
32.74
± 3.86
3.51
± 1.01
1907.83
± 151.27
27.64
± 3.18
70 262032 772.05
± 74.89
730.38
± 35.82
13.27
± 1.10
15.66
± 1.79
1.40
± 0.48
1532.76
± 103.77
17.43
± 1.98
71 262036 7756.15
± 736.74
3407.97
± 228.30
533.12
± 50.83
150.55
± 24.20
11.75
± 1.03
11859.54
± 1018.87
45.69
± 3.02
72 262037 7161.74
± 776.01
2300.09
± 265.61
12.54
± 1.41
202.79
± 35.52
15.63
± 1.85
9692.79
± 1066.16
15.66
± 0.80
73 262044 694.95
± 64.48
313.93
± 21.21
16.01
± 1.00
9.62
± 0.98
0.20
± 0.11
1034.71
± 83.71
19.63
± 1.93
74 262049 1747.75
± 161.08
749.16
± 100.01
143.81
± 16.09
17.98
± 1.41
2.16
± 0.72
2660.86
± 279.13
38.75
± 1.29
75 262050 2529.17
± 263.58
973.73
± 124.64
50.72
± 6.24
51.29
± 5.31
5.07
± 0.52
3609.98
± 399.91
31.08
± 1.87
76 262057 1587.23
± 144.12
628.61
± 72.63
14.36
± 1.54
24.32
± 2.05
1.89
± 0.39
2256.41
± 220.03
19.37
± 1.95
77 262070 2899.72
± 228.78
1012.70
± 48.97
106.6
± 5.25
41.77
± 3.90
3.43
± 0.60
4064.22
± 278.41
18.43
± 5.71
78 262075 4921.87
± 389.66
2323.96
± 179.26
22.73
± 1.28
118.28
± 11.36
9.53
± 0.73
7396.36
± 555.24
23.91
± 2.95
79 262076 8207.53
± 662.86
3318.56
± 198.15
74.34
± 4.57
276.04
± 36.80
19.23
± 0.95
11895.69
± 743.41
27.9
± 3.08
80 264178 3420.25
± 99.52
1329.92
± 135.41
148.07
± 11.80
58.97
± 1.80
6.10
± 0.37
4963.3
± 220.64
63.05
± 33.28
81 264180 4447.28
± 431.07
1930.04
± 240.28
57.13
± 5.99
95.24
± 7.94
11.49
± 0.78
6541.17
± 684.68
28.09
± 1.21
82 276165 609.89
± 54.54
400.04
± 36.88
10.52
± 0.49
9.58
± 0.86
0.41
± 0.27
1030.44
± 88.46
20.02
± 4.00
83 278269 3356.76
± 326.57
1093.71
± 163.91
40.52
± 3.92
48.08
± 4.83
2.19
± 0.28
4541.26
± 494.96
18.96
± 1.68
84 278682 4711.53
± 382.95
1110.76
± 171.65
591.27
± 42.72
64.53
± 6.23
4.90
± 0.99
6482.99
± 543.26
55.17
± 4.43
85 278683 11663.38
± 1257.80
2894.93
± 358.63
703.41
± 76.07
454.01
± 80.97
40.22
± 1.09
15755.96
± 1713.63
16.07
± 2.60
86 278684 8767.59
± 1025.95
2648.30
± 217.99
72.76
± 8.83
347.88
± 63.10
18.52
± 2.29
11855.05
± 1309.80
12.68
± 16.25
87 278685 1316.78
± 102.33
1104.85
± 72.23
5.29
± 0.38
21.07
± 2.20
0.58
± 0.25
2448.57
± 133.23
4.26
± 25.19
88 278727 1266.86
± 129.63
792.83
± 41.70
18.25
± 1.19
18.19
± 1.93
1.31
± 0.06
2097.44
± 143.08
46.29
± 0.53
89 283305 12816.85
± 1468.17
2342.25
± 298.43
96.38
± 9.67
466.24
± 47.87
31.53
± 2.14
15753.25
± 1825.81
31.67
± 1.56
90 283312 4895.8
± 372.14
1234.99
± 26.07
27.01
± 2.09
97.90
± 12.57
4.57
± 0.37
6260.26
± 389.30
17.95
± 2.52
91 283317 5192.73
± 526.49
1330.03
± 147.24
96.69
± 9.80
102.34
± 16.28
9.82
± 0.96
6731.6
± 678.03
14.21
± 1.99
92 289244 5002.57
± 662.49
1517.41
± 255.09
324.15
± 50.58
82.35
± 10.63
5.89
± 1.64
6932.37
± 979.65
44.99
± 1.48
93 291383 1523.63
± 196.73
445.56
± 63.93
14.41
± 1.47
28.15
± 2.76
2.65
± 0.25
2014.41
± 263.61
36.14
± 0.46
94 291423 9723.58
± 1019.92
1730.22
± 246.64
334.58
± 42.10
466.17
± 36.92
30.45
± 2.61
12285.01
± 1346.28
14.88
± 0.14
95 291541 1913.56
± 76.47
976.86
± 113.15
8.10
± 0.22
39.47
± 1.05
2.20
± 0.19
2940.19
± 187.07
21.94
± 1.73
96 293006 7856.62
± 573.90
1144.05
± 52.40
28.61
± 2.51
251.52
± 26.31
13.26
± 0.79
9294.06
± 625.16
17.01
± 2.99
97 293008 6179.58
± 630.56
1514.71
± 91.55
14.66
± 1.52
161.65
± 23.71
12.20
± 2.30
7882.8
± 745.08
22.57
± 1.86
98 293028 8425.24
± 679.54
934.71
± 75.56
32.62
± 2.15
249.98
± 31.27
13.41
± 1.70
9655.96
± 747.74
20.73
± 2.25
99 293085 7402.03
± 706.58
2230.55
± 229.32
93.13
± 23.58
237.61
± 22.52
14.25
± 1.36
9977.56
± 976.05
24.63
± 0.41
100 297120 6933.66
± 428.54
2029.14
± 106.05
449.10
± 30.50
170.32
± 16.06
12.56
± 0.18
9594.78
± 504.88
46.39
± 0.74
101 297172 469.18
± 44.07
163.82
± 11.35
2.03
± 0.14
6.77
± 0.70
0.19
± 0.07
641.98
± 52.73
30.53
± 3.13
102 297174 9182.81
± 914.73
2213.60
± 213.38
203.22
± 20.46
320.68
± 22.55
20.87
± 1.01
11941.19
± 1162.16
18.98
± 0.05
103 299326 9389.02
± 492.80
3128.66
± 149.46
380.53
± 24.92
363.06
± 34.87
43.72
± 4.16
13305
± 612.02
29.43
± 3.52
104 299453 12495.36
± 805.01
4946.47
± 302.76
403.09
± 17.58
534.53
± 51.15
59.07
± 3.24
18438.52
± 970.31
17.77
± 3.55
105 305085 6097.55
± 425.32
2012.43
± 326.01
255.72
± 33.40
154.40
± 12.75
11.19
± 0.80
8531.3
± 792.97
21.49
± 0.56
106 305381 5909.04
± 581.05
1970.40
± 280.71
372.52
± 52.71
212.09
± 26.37
20.16
± 4.22
8484.21
± 941.19
28.34
± 0.29
107 306869 10571.92
± 1141.35
5653.20
± 731.55
1243.88
± 187.47
514.58
± 49.20
34.30
± 2.97
18017.88
± 2108.07
29.77
± 0.94
108 308359 7635.26
± 195.76
3196.07
± 309.54
166.23
± 3.77
218.03
± 9.36
16.94
± 0.74
11232.53
± 421.18
21.61
± 2.78
109 308367 5906.01
± 157.17
1353.42
± 168.61
250.59
± 11.37
198.84
± 7.28
27.66
± 2.92
7736.50
± 246.11
22.85
± 1.54
110 308418 123.76
± 16.36
26.28
± 3.50
1.27
± 0.11
2.97
± 0.20
0.02
± 0.02
154.30
± 20.09
29.52
± 0.16
Con1 Gwailmu 2531.25
± 296.06
1247.67
± 191.43
268.36
± 44.46
40.86
± 4.88
5.31
± 1.24
4093.45
± 536.93
43.31
± 0.54
Con2 Meosjin
maskkalmu
4702
± 522.40
694.89
± 101.45
30.79
± 4.29
112.71
± 11.91
4.72
± 1.30
5545.11
± 641.26
26.91
± 1.04
Con3 Taecheong 6437.09
± 545.29
509.63
± 51.17
7.94
± 1.22
120.97
± 16.81
5.05
± 0.93
7080.67
± 610.67
23.36
± 1.83
Con4 Cheong-
unmu
6210.01
± 775.16
898.02
± 122.53
27.43
± 4.23
146.01
± 17.69
10.01
± 1.78
7291.48
± 920.80
21.66
± 2.47
Con5 Chorongmu 6781.61
± 611.26
532.23
± 62.75
25.82
± 3.70
123.83
± 8.55
8.89
± 0.35
7472.38
± 685.75
30.67
± 0.49
Con6 Mansa-
hyeong
tongmu
7019.84
± 922.97
984.58
± 148.58
44.71
± 7.02
189.20
± 26.21
12.25
± 1.57
8250.57
± 1105.98
26.58
± 0.92
Con7 Togwang
goldeumu
7968.49
± 453.95
991.70
± 64.54
37.75
± 2.59
169.24
± 16.43
8.83
± 0.85
9176.01
± 492.2
21.92
± 3.48
Con8 Baeksi
naltari
7989.39
± 755.68
1144.97
± 126.38
185.86
± 32.79
146.49
± 14.07
10.29
± 1.77
9477.00
± 929.50
26.91
± 0.43
Con9 Syupeo
giljomu
9053.54
± 738.81
1307.13
± 136.26
48.53
± 6.08
212.05
± 17.12
15.36
± 1.48
10636.61
± 894.57
24.51
± 0.20
Con10 Seoho
goldeumu
9247.03
± 706.53
1256.86
± 111.22
59.03
± 8.46
292.94
± 21.42
17.25
± 1.53
10873.12
± 843.35
29.27
± 0.44

zSD means standard deviation.

/media/sites/kjpr/2021-034-06/N0820340609/images/kjpr_34_06_09_A4.jpg
Appendix 4.

MS information of eight glucosinolate standards.

Acknowledgements

The authors would like to acknowledge funding through grants allocated to B. K. from the Rural Development Administration (Project No. 01427702), Republic of Korea. This study was also supported by the 2021 Postdoctoral Fellowship Program (A.D.A.) of the National Institute of Agricultural Sciences, RDA, Republic of Korea.

The authors declare that they have no conflict of interest.

References

1
Afroz, T., O. Hur, N. Ro, J.E. Lee, A. Hwang, B. Kim, A.D. Assefa, J.H. Rhee, J.S. Sung and H.S. Lee. 2021. Evaluation of bioassay methods to assess bacterial soft rot resistance in radish cultivars. J. Life Sci. 31:609-616.
2
Aires, A., V. Mota, M. Saavedra, E. Rosa and R. Bennett. 2009. The antimicrobial effects of glucosinolates and their respective enzymatic hydrolysis products on bacteria isolated from the human intestinal tract. J. Appl. Microbiol. 106:2086-2095. 10.1111/j.1365-2672.2009.04180.x19291240
3
Barillari, J., D. Canistro, M. Paolini, F. Ferroni, G.F. Pedulli, R. Iori and L. Valgimigli. 2005. Direct antioxidant activity of purified glucoerucin, the dietary secondary metabolite contained in rocket (Eruca sativa Mill.) seeds and sprouts. J. Agr. Food Chem. 53:2475-2482. 10.1021/jf047945a15796582
4
Bhandari, S.R., J.S. Jo and J.G. Lee. 2015. Comparison of glucosinolate profiles in different tissues of nine Brassica crops. Molecules 20:15827-15841. 10.3390/molecules20091582726334264PMC6331803
5
Brand-Williams, W., M.E. Cuvelier and C. Berset. 1995. Use of a free radical method to evaluate antioxidant activity. LWT - Food Sci. Tech. 28:25-30. 10.1016/S0023-6438(95)80008-5
6
Cai, Y.X., J.H. Wang, C. McAuley, M.A. Augustin and N.S. Terefe. 2019. Fermentation for enhancing the bioconversion of glucoraphanin into sulforaphane and improve the functional attributes of broccoli puree. J. Functional Foods 61:103461. 10.1016/j.jff.2019.103461
7
Cho, W.K. 2010. A historical study of Korean traditional radish kimchi. J. Korean Soc. Food Cult. 25:428-455.
8
De Nicola, G.R., M. Bagatta, E. Pagnotta, D. Angelino, L. Gennari, P. Ninfali, P. Rollin and R. Iori. 2013. Comparison of bioactive phytochemical content and release of isothiocyanates in selected Brassica sprouts. Food Chem. 141:297-303. 10.1016/j.foodchem.2013.02.10223768361
9
Fahey, J.W., A.T. Zalcmann and P. Talalay. 2001. The chemical diversity and distribution of glucosinolates and isothiocyanates among plants. Phytochemistry 56:5-51. 10.1016/S0031-9422(00)00316-2
10
Geum, N.G., J.H. Yeo, J.H. Yu, M.Y. Choi, J.W. Lee, J.K. Baek and J.B. Jeong. 2021. In vitro immunostimulatory activity of Bok Choy (Brassica campestris var. chinensis) sprouts in RAW264.7 macrophage cells. Korean J. Plant Res. 34:203-215.
11
Gratacós-Cubarsí, M., A. Ribas-Agusti, J.A. García-Regueiro and M. Castellari. 2010. Simultaneous evaluation of intact glucosinolates and phenolic compounds by UPLC-DAD- MS/MS in Brassica oleracea L. var. botrytis. Food Chem. 121:257-263. 10.1016/j.foodchem.2009.11.081
12
Heo, Y., M.J. Kim, J.W. Lee and B. Moon. 2019. Muffins enriched with dietary fiber from kimchi by‐product: Baking properties, physical-chemical properties, and consumer acceptance. Food Sci. Nutr. 7:1778-1785. 10.1002/fsn3.102031139391PMC6526675
13
Hwang, I.M., B. Park, Y.M. Dang, S.Y. Kim and H.Y. Seo. 2019. Simultaneous direct determination of 15 glucosinolates in eight Brassica species by UHPLC-Q-Orbitrap-MS. Food Chem. 282:127-133. 10.1016/j.foodchem.2018.12.03630711096
14
International Board for Plant Genetic Resources (IBPGR). 1990. Descriptors for Brassica and Raphanus, https://www. bioversityinternational.org/e-library/publications/det ail/descriptors-for-brassica-and-raphanus/ (Accessed on 10 Oct, 2021)
15
Ibrahim, M.D., S.B. Kntayya, N. Mohd Ain, R. Iori, C. Ioannides and A.F. Abdull Razis. 2018. Induction of apoptosis and cytotoxicity by raphasatin in human breast adenocarcinoma MCF-7 cells. Molecules 23:3092. 10.3390/molecules2312309230486382PMC6321584
16
Ishida, M., T. Kakizaki, Y. Morimitsu, T. Ohara, K. Hatakeyama, H. Yoshiaki, J. Kohori and T. Nishio. 2015. Novel glucosinolate composition lacking 4-methylthio-3-butenyl glucosinolate in Japanese white radish (Raphanus sativus L.). Theor. Appl. Genet. 128: 2037-2046. 10.1007/s00122-015-2564-326152572
17
Jatoi, S.A., S.U. Siddiqui, M.S. Masood, A. Javaid, M. Iqbal and O.U. Sayal. 2011. Genetic diversity in radish germplasm for morphological traits and seed storage proteins. Pakistan J. Bot. 43:2259-2268.
18
Jeon, B.W., M.H. Oh, E.O. Kim, H.S. Kim and W.B. Chae. 2018. Different vegetative growth stages of kimchi cabbage (Brassica rapa L.) exhibit specific glucosinolate composition and content. Hortic. Envir. Biotech. 59:355-362. 10.1007/s13580-018-0040-0
19
Kakizaki, T., H. Kitashiba, Z. Zou, F. Li, N. Fukino, T. Ohara, T. Nishio and M. Ishida. 2017. A 2-oxoglutarate-dependent dioxygenase mediates the biosynthesis of glucoraphasatin in radish. Plant Physiol. 173:1583-1593. 10.1104/pp.16.0181428100450PMC5338677
20
Kaneko,Y. and Y. Matsuzawa. 1993. Radish (Raphanus sativus L.), p. 487-505. In: G. Kalloo and B.O. Bergh (eds). Genetic improvement of vegetable crops. Pergamon Press, Oxford, England. 10.1016/B978-0-08-040826-2.50039-4
21
Kim, M.J., H.J. Yang, H.Y. Lee, Y.M. Park, D.Y. Shin, Y.H. Lee, Y.G. Kang, T.S. Kim, S.P. Lee and K.H. Park. 2020. Improving effects of Brassica oleraceae L. var. italica sprout extract on alcohol liver dysfunction. Korean J. Plant Res. 33:163-169.
22
Kurina, A.B., D.L. Kornyukhin, A.E. Solovyeva and A.M. Artemyeva. 2021. Genetic diversity of phenotypic and biochemical traits in VIR radish (Raphanus sativus L.) germplasm collection. Plants 10:1799. 10.3390/plants1009179934579332PMC8468841
23
Kwon, S.T., I.Y. and J.H. Shin. 2020. Investigation of defense and vegetative growth related traits of recombinant inbred lines of Brassica rapa. Korean J. Plant Res. 33:615-623.
24
Liang, H., Y. Wei, R. Li, L. Cheng, Q. Yuan and F. Zheng. 2018. Intensifying sulforaphane formation in broccoli sprouts by using other cruciferous sprouts additions. Food Sci. Biotech. 27:957-962. 10.1007/s10068-018-0347-830263824PMC6085252
25
Liu, M., L. Zhang, S.L. Ser, J.R. Cumming and K.M. Ku. 2018. Comparative phytonutrient analysis of broccoli by-products: The potentials for broccoli by-product utilization. Molecules 23:900. 10.3390/molecules2304090029652847PMC6017511
26
Montaut, S., J. Barillari, R. Iori and P. Rollin. 2010. Glucoaphasatin: Chemistry, occurrence, and biological properties. Phytochemistry 71:6-12. 10.1016/j.phytochem.2009.09.02119896154
27
Park, S., M.V. Arasu, M.K. Lee, J.H. Chun, J.M. Seo, S.W. Lee, N.A. Al-Dhabi and S.J. Kim. 2014. Quantification of glucosinolates, anthocyanins, free amino acids, and vitamin C in inbred lines of cabbage (Brassica oleracea L.). Food Chem. 145:77-85. 10.1016/j.foodchem.2013.08.01024128451
28
Rajalingam, N., J.H. Yoon, B. Yoon, N.B. Hung, W.I. Kim, H. Kim, B.Y. Park and S.R. Kim. 2021. Prevalence and molecular characterization of Escherichia coli isolates during radish sprout production in the Republic of Korea. Appl. Biol. Chem. 64:1-8. 10.1186/s13765-021-00597-3
29
Rhee, J.H., S. Choi, J.E. Lee, O.S. Hur, N.Y. Ro, A.J. Hwang, H.C. Ko, Y.J. Chung, J.J. Noh and A.D. Assefa. 2020. Glucosinolate content in Brassica genetic resources and their distribution pattern within and between inner, middle, and outer leaves. Plants 9:1421. 10.3390/plants911142133114129PMC7690824
30
Scholl, C., B.D. Eshelman, D.M. Barnes and P.R. Hanlon. 2011. Raphasatin is a more potent inducer of the detoxification enzymes than its degradation products. J. Food Sci. 76: C504-C511. 10.1111/j.1750-3841.2011.02078.x21535821
31
Singh, B., T. Koley, P. Karmakar, A. Tripathi, B. Singh and M. Singh. 2017. Pigmented radish (Raphanus sativus): Genetic variability, heritability and interrelationships of total phenolics, anthocyanins and antioxidant activity. Indian J. Agr. Sci. 87: 1600-1606.
32
Suzuki, I., Y.M. Cho, T. Hirata, T. Toyoda, J.I. Akagi, Y. Nakamura, A. Sasaki, T. Nakamura, S. Okamoto and K. Shirota. 2017. Toxic effects of 4‐methylthio‐3‐butenyl isothiocyanate (Raphasatin) in the rat urinary bladder without genotoxicity. J. Appl. Toxicol. 37:485-494. 10.1002/jat.338427633481
33
Suzuki, I., Y.M. Cho, T. Hirata, T. Toyoda, J.I. Akagi, Y. Nakamura, E.Y. Park, A. Sasaki, T. Nakamura and S. Okamoto. 2016. 4-Methylthio-3-butenyl isothiocyanate (raphasatin) exerts chemopreventive effects against esophageal carcinogenesis in rats. J. Toxicol. Pathol. 29:237-246. 10.1293/tox.2016-003727821908PMC5097966
34
International Union for the Protection of new Varieties of plants (UPOV). 2021. For distictess, uniformity and stability, https://www.upov.int/edocs/mdocs/upov/en/twv/44/tg_63_ 7_proj_4_and_64_7_proj_3.pdf (Accessed on 10 Oct, 2021).
35
Vavilov, N.I. 1926. Studies on the origin of cultivated plants. Bull. Appl. Bot. Plant Breeding 14:1-245.
36
Wang, Q., Y. Wang, H. Sun, L. Sun and L. Zhang. 2020. Transposon-induced methylation of the RsMYB1 promoter disturbs anthocyanin accumulation in red-fleshed radish. J. Exp. Bot. 71: 2537-2550. 10.1093/jxb/eraa01031961436PMC7210773
37
Yi, G., S. Lim, W.B. Chae, J.E. Park, H.R. Park, E.J. Lee and J.H. Huh. 2016. Root glucosinolate profiles for screening of radish (Raphanus sativus L.) genetic resources. J. Agr. Food Chem. 64:61-70. 10.1021/acs.jafc.5b0457526672790
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