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Journal of the Science of Food and Agriculture

J Sci Food Agric 86:14811488 (2006)

Antioxidant capacity and secondary


metabolites in four species of Andean
tuber crops: native potato (Solanum sp.),
mashua (Tropaeolum tuberosum Ruiz &

Pavon),
Oca (Oxalis tuberosa Molina) and
ulluco (Ullucus tuberosus Caldas)
David Campos,1 Giuliana Noratto,2 Rosana Chirinos,1 Carlos Arbizu,3 Willian Roca3
and Luis Cisneros-Zevallos2
1 Instituto

de Biotecnologa, Universidad Nacional Agraria-La Molina, Lima 12, Peru


of Horticultural Sciences, Texas A&M University, College Station, TX 77843-2133, USA
3 International Potato Center, Lima 12, Peru
2 Department

Abstract: Four species of edible tubers endemic to and domesticated in the Andes, native potato (Solanum sp.),

mashua (Tropaeolum tuberosum Ruiz & Pavon),


oca (Oxalis tuberosa Molina) and ulluco (Ullucus tuberosus
Caldas), were studied for their antioxidant capacity and associated secondary metabolites. The antioxidant
capacity was measured using ABTS radicals and total phenolics, carotenoids, anthocyanin, betaxanthin and
betacyanin content were also characterized. The antioxidant capacity found in the crops studied ranged from 483
to 9800 g trolox equiv. g1 , phenolics ranged from 0.41 to 3.37 mg chlorogenic acid equiv. g1 , anthocyanins ranged
from 0.08 to 2.05 mg cyanidin 3-glucoside g1 and carotenoids ranged from 1 to 25 g -carotene g1 . The content of
bioactive compounds was high and variable between crops and within the genotypes studied. In general, mashua
tubers showed the highest antioxidant capacity and phenolic, anthocyanin and carotenoid content compared with
other crops. Ulluco was the only crop that contained betalains in the acid form of betaxanthins (2296 g g1 ) and
betacyanins (64 g g1 ) with no presence of carotenoids or anthocyanins. This is the first publication regarding the
antioxidant capacity of and associated secondary metabolites in Andean tubers. This information can be useful
in the identification of Andean tubers species and genotypes with potential value as a novel dietary source of
antioxidants for food, and also for medicinal use.
2006 Society of Chemical Industry

Keywords: antioxidants; Andean tuber crops; potato; mashua; oca; ulluco

INTRODUCTION
There is a continuous search for new plant compounds with antioxidant potential. Interest in natural antioxidants has increased considerably in recent
years.1 4 Antioxidants, which can neutralize free radicals, may be of central importance in the prevention
of cancer and cardio- and cerebrovascular diseases.5 9
Many natural antioxidants exhibit a wide range of
biological effects, including antibacterial, antiviral,
anti-inflammatory, antiallergic, antithrombotic and
vasodilatory activity.10 The Andean region is well
known for its great genetic diversity in different types of
crops, which unfortunately have been poorly studied.
Andean crops show variability in colors, forms, sizes,
primary nutrient constituents and bioactive secondary
metabolites.
People from the Andean region have utilized native
potato (Solanum sp.), mashua (Tropaeolum tuberosum

Ruiz & Pavon),


oca (Oxalis tuberosa Molina) and ulluco
(Ullucus tuberosus Caldas) tubers for their nutritional
and medicinal properties since ancient times. It is
thought that the health-related properties of Andean
tuber crops claimed from folklore use could be in part
attributed to the antioxidants present in these crops.
However, little is known about the chemical nature
and identity of the bioactive compounds present.
Hence there is a need for scientific data on the
antioxidant content of these Andean crops in order
to increase our understanding of their role in the
diet and in reducing chronic diseases. These initial
steps may lead to an increased antioxidant intake
by breeding Andean crops with higher antioxidant
activity.
There have been a few attempts at quantifying
the nutritional value of Andean tubers,11,12 but this
study is the first attempt to measure accurately the

Correspondence to: Luis Cisneros-Zevallos, Department of Horticultural Sciences, Texas A&M University, College Station, TX 77843-2133, USA
E-mail: lcisnero@taexgw.tamu.edu
(Received 17 February 2005; revised version received 26 September 2005; accepted 20 February 2006)
Published online 15 June 2006; DOI: 10.1002/jsfa.2529

2006 Society of Chemical Industry. J Sci Food Agric 00225142/2006/$30.00

D Campos et al.

antioxidant capacity and related bioactive compounds


of a wide germplasm of different Andean tubers.
The objective of this study was to provide new
data regarding Andean tuber crops as a source
of antioxidant compounds and compare them with
other commercial crops. The information obtained
should stimulate an increase in the evaluation and
conservation of tuber diversity within the Andean
region and in the identification of these crops as new
sources of functional foods.

MATERIALS AND METHODS


Plant material
Fifteen native potato (Solanum sp.), 14 oca genotypes
(Oxalis tuberosa Molina), 15 ulluco (Ullucus tuberosus
Caldas) and 11 mashua (Tropaeolum tuberosum Ruiz &
genotypes were supplied by the International
Pavon)
Potato Center (CIP) (Lima, Peru). The tubers were
harvested during June 2002 from CIPs experimental
fields in Huancayo (37003800 m), Peru. Strawberry
and carrots were purchased from a local market in
Lima and used as reference crops. Tuber samples
were analyzed for total phenolics (TPH), anthocyanins
(ACY), carotenoids (CTC), betaxanthins (TBX),
betacyanins (TBC), hydrophilic antioxidant capacity
(HAC) and lipophilic antioxidant capacity (LAC).
Strawberries were analyzed for ACY and TPH and
carrots for TCT; these two crops were used as
reference crops for comparison purposes. All samples
were frozen and stored at 20 C until the time of
analysis. Samples were taken from the middle section
in slices which included skin and flesh in the analysis to
keep the original ratio between skin and flesh present
in the tuber. The analyses were run in triplicate for
each tuber using three tubers per genotype.
Chemicals
All solvents and other chemicals were of
analytical grade and obtained from Merck
(Darmstadt, Germany), J.T. Baker (Phillipsburg,
NJ, USA) and Mallinckrodt (Phillipsburg, NJ,
USA). 2,2 -Azinobis(3-ethylbenzthiazoline-6-sulfonic
acid (ABTS) and FolinCiocalteu reagent (Catalog
#F9252) were purchased from Sigma Aldrich (St
Louis, MO, USA).
Total phenolic compounds (TPH)
Total phenolics were determined using the
FolinCiocalteu reagent following the procedure
reported by Swain and Hillis.13 A 5-g sample was
homogenized with 20 mL of 95% ethanol to a uniform
consistency using an Ultra-Turrax homogenizer and
left at 4 C for 24 h before filtration. An aliquot of
extract (0.5 mL) was diluted with 8 mL of water.
Simultaneously, a blank sample was prepared with
95% ethanol and treated in the same way as the
samples. The FolinCiocalteu reagent was diluted
with water (1:7) and 0.5 mL were added to the diluted
extracts, vortex mixed and allowed to react for 3 min.
1482

At 3 min, 1 mL of 0.5 mol L1 Na2 CO3 was added


and allowed to react for 10 min. The absorbance was
measured at 725 nm until a constant reading was
reached. Chlorogenic acid was used as standard for
the calibration curve and TPH were expressed as mg
of chlorogenic acid equiv. g1 fresh weight. A Gensys5 UVvisible spectrophotometer (Milton Roy, New
York, USA) was used for absorbance readings.
Total anthocyanins (ACY)
The method reported by Fuleki and Francis14 was
used for ACY determination. A 5-g sample and
15 mL of solvent (85:15 95% ethanol1.5 mol L1
HCl) were homogenized as described above and left
at 4 C for 24 h before filtration. A 2-mL volume
of extract was transferred to a graduated cylinder
and anthocyanin solvent was added to obtain a final
volume of 100 mL. Hexane was added to remove
any carotenoids present. Spectrophotometric readings
at 535 nm were taken, subtracting the absorbance at
700 nm (due to turbidity). ACY were expressed as mg
cyanidin 3-glucoside equiv. g1 fresh weight, using a
molar extinction coefficient15 of 25 965 L mol1 cm1
and a molecular weight of 449 g mol1 .
Total carotenoids (TCT)
The method reported by Talcott and Howard16 was
used for measuring TCT. A 2-g sample with 20 mL of
acetoneethanol (1:1) solution containing 200 mg L1
BHT was homogenized as described above before
filtration. The filtrate was transferred into a graduated
cylinder and solvent added to a final volume of
100 mL. A 50-mL volume of hexane and 25 mL
of H2 O were added and shaken vigorously before
standing for 30 min to allow separation of phases
to occur. The spectrophotometer was blanked with
hexane and the absorbance of the hexane phase
was measured at 470 nm. -Carotene was used as
a standard for the calibration curve and TCT was
expressed as g -carotene equiv. g1 fresh weight.
Betaxanthins (TBX) and betacyanins (TBC)
The method adapted from Cai and Corke17 was
used for measuring betalains. A 5-g sample and
20 mL of solvent (McIllvaine buffer, pH 5.2) were
homogenized for 2 min as described above. Solvent
was added to a final volume of 50 mL before
filtration. The spectrophotometer was blanked with
McIllvaine buffer. The absorbance of the extract
was measured at 476 nm for betaxanthin content
(orangeyellow pigment) and 536 nm for betacyanin
content (purplered pigment). The content of total
betaxanthins and betacyanins was calculated using
absorptivity values, E 1% 1cm , of 750 and 1120,
respectively. Results were expressed as mg TBX or
TBC g1 fresh weight.
Determination of antioxidant capacity
Antioxidant capacity was determined by the ABTS
method adapted from Arnao et al.18 A 5-g sample and
J Sci Food Agric 86:14811488 (2006)
DOI: 10.1002/jsfa

Antioxidants in Andean tuber crops

J Sci Food Agric 86:14811488 (2006)


DOI: 10.1002/jsfa

705841

704463

707132

705263

703985

705024

703286

706819

0
704353

0
705468

1000

702961

703279

2000

703825

703844

3000

HAC (ug TE g-1)

5000

704481

TPH or ACY (mg g-1)

HAC

4000

Figure 1. Total phenolic content (TPH), anthocyanins (ACY) and


hydrophilic antioxidant capacity (HAC) of native potato tubers
(Solanum sp.).

11500

12
ACY

HAC

9500

-500

M6COL2C

ARB-5576

ARB-5241

DP-02-24

1500

ARV-5366

DP-02-15

3500

AGM-5109

AVM-5562

5500

DP-02-07

DP-02-23

7500

DP-02-03

HAC (ug TE g-1)

TPH

10

Figure 2. Total phenolic content (TPH), anthocyanins (ACY) and


hydrophilic antioxidant capacity (HAC) of mashua tubers.

(Tropaeolum tuberosum Ruiz & Pavon).

6500
TPH

ACY

5500

HAC

4500

2.5

3500

2
2500

1.5

1500

HAC (ug TE g-1)

3.5

500

0.5

-500
O-018-83

AAQ-5477

MU-31

AMM-5223

O-116-84

PICA-HI-92 OC

COC-537

DP-01-46

AJA-5252

ATT-5466

AJA-5245

O-266-85

0
AJA-5270

Total phenolic content (TPH)


Our results indicate that the TPH content for
native potato ranged from 0.64 to 2.32 mg g1
(Fig. 1). Genotypes 707 132, 704 463 and 705 841
had the highest TPH contents with 2.32, 2.09
and 1.9 mg g1 , respectively. These values are higher
than those reported previously for purple potatoes20
(0.761.27 mg g1 ). In mashua tubers, the TPH
ranged from 0.92 to 3.37 mg g1 (Fig. 2). Genotypes
ARB-5241, DP-02-24 and AGM-5109 had the highest
TPH with 3.37, 3.05 and 2.75 mg g1 , respectively.
Purple mashua genotypes presented higher TPH
values, whereas lower values of TPH were found in

ACY

ARB-5054

RESULTS AND DISCUSSION


The overall average moisture content of the genotypes
studied in native potatoes, mashua, oca and ulluco
tubers was 71.5 3.4, 89 2.2, 83 1.9 and
86.7 1.7%, respectively, indicating a small variation
of moisture content among the genotypes studied in
each crop. In general, results expressed on dry or wet
basis did not alter the overall ranking for each crop in
relation to TPH, ACY, TCT, HAC and LAC in this
study. We consider it meaningful to present the data
on a wet or fresh basis since that is the way in which
these crops are consumed and the way in which most
references are available in the literature.

TPH

TPH or ACY (mg g-1)

Statistical analysis
SPSS for Windows version 11.0 was used for
statistical analysis. Pearson correlation at the level
of = 0.01 and analysis of variance (ANOVA) with
mean comparisons using Tukeys multiple range test
at = 0.05 were performed. Results are expressed as
average standard deviation (SD).

6000

TPH or ACY (mg g-1)

25 mL of methanol were homogenized as described


above and left at 4 C for 24 h before filtration.
An aliquot of this extract was taken for measuring
the hydrophilic antioxidant capacity (HAC). The
pellet was mixed with 25 mL of dichloromethane
and shaken for 15 min before filtration. An aliquot
of the yelloworange supernatant was taken for
measuring of lipophilic antioxidant capacity (LAC).
A 150 l volume of extract was mixed with 2.85 mL of
ABTS solution (1.1 absorbance, 734 nm) prepared
as described by Awika et al.19 This mixture was
allowed to react at 20 C until a steady absorbance
was reached. Simultaneously, a 150-l aliquot of
methanol was treated in the same way as the sample
and used as a control. The spectrophotometer was
blanked with methanol and the decrease in absorbance
due to antioxidant activity was recorded at 734 nm.
Antioxidant capacity was calculated from a calibration
curve developed for Trolox, providing a relative
antioxidant capacity of the extracts compared with
this standard and expressed as g TE (trolox equiv.)
g1 fresh weight.

Figure 3. Total phenolic content (TPH), anthocyanins (ACY) and


hydrophilic antioxidant capacity (HAC) of oca tubers (Oxalis
tuberosa Molina).

yellow mashua genotypes. The TPH content of ARB5241 was comparable to that of strawberries, used as
a reference (3.35 mg g1 ). For oca tubers, the TPH
ranged from 0.71 to 1.32 mg g1 (Fig. 3). Genotypes
O-018-83, MU-31 and AAQ-5477 showed the
highest TPH values with 1.32, 1.31 and 1.26 mg g1 ,
1483

D Campos et al.
2200
TPH

1.4

TBX

HAC
1700

1.2
1

1200

0.8
700

0.6
0.4

200

HAC (ug TE g-1)

TPH or TBX (mg g-1)

1.6

0.2
-300
U-108-84

U-034-83

AJA-5275

DPA-03-23

PRODEKON-16

MH-296

DPA-03-43

AQP-5454

CLC-004

U-09-0122

CLC-053

ARV-5337

PRODEKON-14

U-09-0124

AMM-5142

Figure 4. Total phenolic content (TPH), betaxanthines (BTX) and


hydrophilic antioxidant capacity (HAC) of ulluco tubers (Ullucus
tuberosus Caldas).

respectively. Oca genotypes with the highest TPH


were purple, whereas lower TPH values were found
in yellow genotypes. Ulluco tubers had the lowest
TPH content compared with the other crops studied.
The TPH of ulluco tubers ranged from 0.41 to
0.77 mg g1 (Fig. 4), with genotypes U-10884, AJA5275 and U-09-0122 showing the highest phenolic
content with 0.77, 0.63 and 0.61 mg g1 , respectively.
The phenolics identified previously in ulluco include
rutin, narcissin and kaempferol 3-O-(2 ,6 -di-O--Lrhamnopyranosyl)--D-glucopyranoside.21 In general,
the TPH range values for the crops studied followed
the descending order mashua native potato oca >
ulluco.
Total anthocyanins (ACY)
The ACY in the pigmented native potato tubers ranged
from 0.08 to 0.8 mg g1 and was only present in some
genotypes (Fig. 1). Genotypes 704 463 and 707 132
showed higher levels of ACY with 0.8 and 0.59 mg g1 ,
respectively. The ACY values were comparable to
those reported previously20 for purple flesh potatoes,
which ranged from 0.11 to 0.6 mg g1 , and higher than
the ACY content in strawberries (0.4 0.13 mg g1 ,
in this study). The high ACY content of native
potatoes indicates that these red and purple flesh tuber
genotypes may be a novel source of natural colorants.
The ACY may constitute a significant fraction of the
TPH. For example, the ACY/TPH ratio was highest
(0.38) in genotype 704 463 and ranged between 0.09
and 0.38 for all pigmented native potato samples.
The ACY in mashua pigmented genotypes ranged
from 0.5 to 2.05 mg g1 (Fig. 2). This ACY content
is higher than those reported22 for radish cv.
Fuego (0.30 mg g1 ), red cabbage (0.25 mg g1 ),
strawberry (0.150.3 mg g1 ) and red raspberry
(0.30.4 mg g1 ). The highest amount was found in
genotype DP-02-24, which is in the range reported for
blueberry,23 1.383.85 mg g1 . The ACY in mashua
tubers seems to be a significant component of the
TPH in the pigmented genotypes. For example, the
ACY/TPH fraction ranged between 0.3 and 0.67.
1484

For oca pigmented tubers, the ACY ranged from


0.14 to 1.3 mg g1 (Fig. 3). The highest amount was
found in MU-31 and seems to be concentrated mostly
in the tuber skin. For pigmented tubers, the ACY/TPH
fraction ranged from 0.14 to 0.9. The ACY/TPH
fraction was low (0.14) in genotype PICA-HI-92OC,
owing to the relatively high TPH values, whereas for
genotype MU-31, the fraction was high (0.9) owing
to the high ACY content. On the other hand, our
results showed that ulluco tubers do not contain
anthocyanins. In general, the ACY range values of
the crops studied followed the descending order
mashua oca native potato. The presence or not of
ACY and the differing proportions of ACY observed
indicate that the genotypes studied in each type of
crop would have different qualitative and quantitative
phenolic profiles.
Total carotenoids (TCT)
The TCT in native potatoes ranged from 2 to
5 g g1 (Table 1), these values being higher than
those reported previously for commercial varieties,24,25
which are in the range 0.273.43 g g1 . The
705 468 genotype had the highest carotenoid content
with 5 g g1 . Interestingly, only one red pigmented
genotype (705 024) presented carotenoids, phenolics
and anthocyanins in the same tuber. In general, tubers
with carotenoids tended visually to correlate with
flesh yellow intensity. Violaxanthin is considered the
main potato carotenoid reported in previous studies.
followed by lutein, antheraxanthin and others.26
Lutein has attracted interest since high blood serum
levels are correlated with a reduced risk for age-related
macular degeneration in humans (AMD).25,27
In mashua tubers, the TCT ranged from 1 to
25 g -carotene g1 (Table 2). Genotypes ARB5576, M6COL2C and DP-0207 had the highest
carotenoid contents with 25, 23 and 21 g g1 ,
respectively. The carotenoid content of mashua
tubers is relatively high compared with commercial
potatoes24,25 and those found in native potatoes in this
study, and also the carotenoid content in papaya28
(4.08 g g1 ). However, TCT in mashua are lower
than those reported28 for tomato (56210 g g1 ),
mango (74.3 g g1 ) and carrot (90 16 g g1 in this
study).
For oca tubers, the TCT ranged from 2 to 25 g
-carotene g1 (Table 3). Genotypes AJA-5245 and
AJA-5270 had the highest carotenoid content with
25 and 17 g -carotene g1 , respectively. Genotype
AAQ-5477 showed high ACY, TCT and TPH content
among all oca genotypes studied. In the case of ulluco,
the results indicate that these tubers do not contain
carotenoids in the pigmented yellow tissue. According
to the present results, the carotenoid content range
values for the crops studied followed the descending
order mashua oca native potato.
Betaxanthins (TBX) and betacyanins (TBC)
By using absorption spectra, the aqueous solubility
properties and the response to alkaline (change to
J Sci Food Agric 86:14811488 (2006)
DOI: 10.1002/jsfa

Antioxidants in Andean tuber crops


Table 1. Total carotenoid content (TCT) and lipophilic antioxidant capacity (LAC) in 15 native potato (Solanum sp.) genotypes

Genotype
707 132
705 024
705 841
704 463
703 286
703 825
705 263
703 985
704 353
702 961
705 468
706 819
703 279
704 481
703 844
a
b

Common
name
Yana Shiri
Pachacona
Unknown
Gogon Magash
Yana Pituwayaka
China Runtush
Chaucha
Runtu
Puna
Garhuash Pashon
Huasa Amarilla
Tablera Jubalena
Seda Monilla
Amarilla
Anil Papa

Species
S. curtilobum
S. tuberosum subsp. tuberosum
S. tuberosum subsp andigena
S. tuberosum subsp andigena
S. stenotomum
S. goniocalyx
S. phureja
S. goniocalyx
S. tuberosum subsp andigena
S. goniocalyx
S. goniocalyx
S. tuberosum subspp. andigena
S. goniocalyx
S. goniocalyx
S. stenotomum

Color of
flesh/skina

Moisture
(%)b

TCT
(g g1 )b

LAC
(g TE g1 )b

P/P
P/P
R/R
P/P
P/Y
Y/Y
Y/Y
Y/Y
Y/Y
Y/Y
Y/Y
Y/Y
Y/Y
Y/Y
Y/Y

78 3.9f
76 1.6e,f
75 1.0d,e,f
75 1.2d,e,f
74 0.7c,d,e,f
72 3.9c,d,e,f
72 4.9c,d,e,f
70 0.7c,d,e
70 2.9c,d,e
70 0.5c,d,e
69 3.3c,d,e
69 1.7c,d,e
69 3.0c,d,e
68 1.5c,d
66 2.8c

ND
4 0.1d,e,f
ND
ND
ND
4 1.3d,e,f
4 1d,e,f
4 1e,f
2 0c,d
2 1c,d,e
5 1f
4 0d,e,f
3 1c,d,e,f
3 0c,d,e,f
4 1d,e,f

321 15e,f
211 7c,d,e
152 35c,d
131 26c,d
357 30f
133 53c,d
239 102c,d,e,f
155 82c,d
199 76c,d,e
170 40c,d
249 30c,d,e,f
115 28c
125 19.21c,d
265 28d,e,f
361 13f

P, purple; Y, yellow; R, red.


Mean SD (n = 3). Means within a column with the same superscript letter are not significantly different ( = 0.05). ND, not detected.

Table 2. Total carotenoid content (TCT) and lipophilic antioxidant

capacity (LAC) in 11 mashua (Tropaeolum tuberosum Ruiz & Pavon)


genotypes

Genotype

Color of
flesh/
skina

Moisture
(%)b

TCT
(g g1 )b

LAC
(g TE g1 )b

AVM-5562
DP-02-07
DP-02-15
M6COL2C
DP-02-23
AGM-5109
DP-02-03
DP-02-24
ARB-5576
ARB-5241
ARV-5366

Y/Y
Y/Y
Y/Y
Y/Y
Y/Y
P/Y
Y/Y
P/P
Y/Y
P/Y
Y-P/P

92 1.6c
90 1.0c,d
90 1.9c,d,e
90 1.6c,d,e
90 1.6c,d,e
89 1.2c,d,e
87 2.8c,d
87 1.3c,d
87 1.4c,d
85 1.7c
86 0.6c

14 3d,e
21 3d,e
17 1d,e
23 6e
13 6d,e
18 0d,e
21 4d,e
ND
25 9e
10 1c,d
1 0c

217 37.7e,f
221 13.0e,f
186 9.6d,e
279 15.0f
93 22.85c
128 56.1c,d
224 24.7e,f
ND
218 12.8e,f
202 19.3d,e,f
225 44e,f

P, purple; Y, yellow; R, red.


Mean SD (n = 3). Means within a column with the same superscript
letter are not significantly different ( = 0.05). ND, not detected.

Table 3. Total carotenoid content (TCT) and lipophilic antioxidant


capacity (LAC) in 14 oca (Oxalis tuberosa Molina) genotypes

Genotype
PICA-HI92OC
O-116-84
O-266-85
ARB-5054
ATT-5466
COC-537
MU-31
AMM-5223
AJA-5245
AAQ-5477
AJA-5270
O-018-83
DP-01-46
AJA-5252

Color of
flesh/
skina

Moisture
(%)b

TCT
(g g1 )b

LAC
(g TE g1 )b

Y-R/P

82 1.4c,d,e

8 0c,d

165 23c,d,e

Y-P/P
Y/Y
Y/Y
Y-R/P
Y-P/P
Y-P/P
Y-R/P
Y/Y
Y-P/P
Y/Y
P-Y/P
Y-P/P
Y/Y

80 1.7c,d
82 2.0c,d,e
84 1.5c,d,e
84 0.7c,d,e
85 2.6e
85 0.8e
80 1.0c
84 0.2c,d,e
82 0.8c,d,e
84 0.8c,d,e
85 1.3d,e
81 1.3c,d,e
84 2.4d,e

7 1c,d
13 2d,e
14 1d,e
5 1c,d
2 1c
3 1c
3 1c
25 4f
11 9c,d,e
17 2e,f
3 1c
3 1c
10 2c,d,e

126 44c,d
164 39c,d,e
101 4c,d
219 33d,e,f
268 41e,f
76 24c
69 58c
127 34c,d
320 59f
90 25c,d
181 30c,d,e
135 79c,d,e
107 72c,d

a stable yellow color) and acidic conditions (color


disappearance on boiling),29 it was found that the
pigments in ulluco correspond to betalains in the base
form of betacyanins (red pigment, max 535540 nm)
and the acid form of betaxanthins (yellow pigment,
max 453475 nm). The results indicate that TBX
in ulluco tubers ranged from 22 to 96 g g1 (Fig. 4).
The highest amount was found in genotypes CLC-004
and U-09-0122 with 96 and 83 g g1 , respectively.
In general, these pigments have been shown to be
a potential source of both natural antioxidants and
natural colorants in Amaranthaceae.30 Only genotype
AQP-5454, which corresponds to a red skin ulluco
tuber- presented betacyanins (TBC = 64 g g1 ).
Hydrophilic antioxidant capacity (HAC)
The HAC obtained for native potatoes ranged from
860 to 3780 g TE g1 (Fig. 1). Genotypes 705 841,
J Sci Food Agric 86:14811488 (2006)
DOI: 10.1002/jsfa

P, purple; Y, yellow; R, red.


Mean SD (n = 3). Means within a column with the same superscript
letter are not significantly different ( = 0.05).
b

704 463 and 707 132 showed the highest HAC values
with 3780, 3369 and 2473 g TE g1 , respectively.
Potatoes are known to contain water-soluble phenolic
antioxidants that act as radical scavengers such as
quercetin and chlorogenic acid.31 We found that
increasing TPH in tubers showed a trend of increasing
HAC values (Fig. 1), despite the low correlation
between HAC and TPH (r 2 = 0.45, P = 0.00). A
high correlation between HAC and TPH for different
genotypes in a certain type of crop would only be
possible if the genotypes have phenolic compounds
with similar antioxidant properties (e.g. similar protondonor properties). Since the correlation obtained
is low, we hypothesize that the studied native
potatoes had different phenolic profiles (qualitative,
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D Campos et al.

quantitative or both) with different antioxidant


properties. Furthermore, when HAC is expressed on
a phenolic basis (defined as the HAC/TPH ratio in
this study), this specific HAC ranged from 1066 to
2294 mg TE g1 chlorogenic acid equiv. This indicates
that the phenolics present in some of the genotypes
showed a higher antioxidant capacity to stabilize a
greater number of free radicals than others. The
specific HAC values obtained are comparable to those
reported previously for blueberries (6851966 mg TE
g1 phenolics) and higher than for blackberries32
(532 mg TE g1 phenolics).
For mashua tubers, the HAC ranged from 955 to
9800 g TE g1 (Fig. 2). Genotypes ARB-5241, DP02-24 and ARV-5366 showed the highest HAC values
with 9800, 9309 and 7867 g TE g1 , respectively.
Our results indicate that mashua genotype ARB5241 is comparable to blueberry32 (cultivar premier,
HAC = 9572 g TE g1 ), which is considered one of
the fruits with the highest antioxidant capacity.33 35
Again, for mashua tubers the antioxidant capacity
could be related to the ACY and TPH content
according to Fig. 2. The low ACY correlation with
HAC (r 2 = 0.48, P = 0.11); and the higher correlation
between TPH and HAC (r 2 = 0.84, P = 0.00) are
most likely due to the presence of different phenolic
profiles in mashua tubers, as in the case of native
potatoes. When the HAC is expressed on a phenolic
basis, the values obtained ranged from 729 to 3052 mg
TE g1 chlorogenic acid equiv., which could be
related to these different phenolic profiles. The highest
values were found in genotypes DP-02-24 (3052 mg
TE g1 chlorogenic acid equiv.) followed by ARB5241 (2908 mg TE g1 chlorogenic acid equiv.). The
specific HAC values for mashua are higher than those
observed for blueberries.32
In the case of oca tubers, HAC ranged from 1637
to 4771 g TE g1 (Fig. 3). Genotypes O-018-83,
AAQ-5477 and MU-31 had the highest HAC values
with 4771, 4396 and 3994 g TE g1 , respectively.
Genotype O-018-83 had a HAC value of 70%
of that in Rabbiteye blueberry cultivars with high
HAC (average 6900 g TE g1 ).32 Once again, the
antioxidant capacity could be related mainly to the
TPH content (Fig. 3). For oca tubers, the correlation
between HAC and TPH was high and significant
(r 2 = 0.75, P = 0.00), indicating in this case that the
phenolics present in oca tubers could have similar
antioxidant properties. When HAC is expressed on
a phenolic basis, a range from 1935 to 3614 mg
TE g1 chlorogenic acid was found, which is higher
than those reported for blueberries and blackberries.32
These specific HAC values are comparable to those
found in mashua, indicating the potential that these
crops have as a novel source of phenolic compounds
with high antioxidant capacity.
Ulluco tubers presented a HAC range from 483 to
1524 g TE g1 (Fig. 4). Genotypes U-108-84, AJA5275 and U-034-83 showed the highest HAC values
with 1524, 1372 and 1183 g TE g1 , respectively.
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When HAC is expressed on a phenolic basis, the


highest specific HAC among the ulluco genotypes was
found in genotype DP-03-43 with 2322 mg TE g1
chlorogenic acid equiv. A low correlation between
HAC and TPH was observed (r 2 = 0.64, P = 0.00),
most likely due to different phenolic profiles among
ulluco cultivars. In general, the trend observed was
an increased antioxidant capacity for genotypes with
higher phenolic content (Fig. 4). Among the phenolics
present in ulluco,21 the flavonoid kaempferol has been
reported to exhibit strong antioxidant activity36,37 and
to inhibit hemolysis, lipid peroxidation and superoxide
radical generation.38 On the other hand, HAC and
TBX were not correlated, suggesting that the TBX
does not contribute to the HAC in ulluco. According
to the results obtained, the HAC range values for
the crops studied followed the descending order
mashua oca native potato ulluco.
Lipophilic antioxidant capacity (LAC)
In native potatoes, the LAC ranged from and 115 to
361 g TE g1 (Table 1). Genotypes 703 844, 703 286
and 707 132 showed the highest LAC values with 361,
357 and 321 g TE g1 , respectively. Interestingly, two
genotypes lacking carotenoids showed LAC properties
suggesting the presence of lipophilic compounds other
than carotenoids with radical scavenging activity.
Among the native potatoes, genotypes 705 841,
704 463 and 707 132 showed the highest total
antioxidant capacity (lipophilic + hydrophilic) with
3932, 3500 and 2794 g TE g1 , respectively. The
lipophilic fraction of native potatoes contributed only
3.724.5% of the total antioxidant capacity values.
For mashua tubers, the LAC ranged from 93 to
279 g TE g1 (Table 2). Genotypes M6COL2C,
ARV-5366 and DP-02-03 showed the highest LAC
values with 279, 225 and 224 g TE g1 , respectively.
In mashua, LAC was observed only in genotypes that
had carotenoids. Genotypes ARB-5241 and AGM5109 presented LAC values (1346 and 1163 g TE g1
DW, respectively) comparable to tomato39 (1425 g
TE g1 DW). The correlation between LAC and
TCT was very low (r 2 = 0.14, P = 0.058), suggesting
that the carotenoid profiles between genotypes were
different. In general, genotypes ARB-5241, DP-0224 and ARV-5366 had the highest total antioxidant
capacity (lipophilic + hydrophilic) with 10 002, 9309
and 8092 g TE g1 , respectively. The lipophilic
fraction contributed 219% to the total antioxidant
capacity values for mashua tubers.
The LAC of oca tubers ranged from 69 to 320 g TE
g1 , with genotypes AAQ-5477, COC-537 and ATT5466 showing the highest LAC values with 320, 268
and 219 g TE g1 , respectively (Table 3). There is no
correlation between LAC and TCT in oca tubers, most
likely owing to different profiles of carotenoids present
in the different genotypes. Genotypes O-01883,
AAQ-5477 and MU-31 showed total antioxidant
capacities (lipophilic + hydrophilic) of 4952, 4716 and
4070 g TE g1 , respectively. The lipophilic fraction
J Sci Food Agric 86:14811488 (2006)
DOI: 10.1002/jsfa

Antioxidants in Andean tuber crops

Figure 5. Andean tubers with high antioxidant capacity: (A) native potato 707 132; (B) mashua ARB-5241; (C) oca O-018-83; (D) ulluco U-108-84.

contributed 1.910.2% to the total antioxidant


capacity values for oca tubers.
For ulluco tubers, our results indicate that they do
not present LAC for any of the genotypes studied. In
general, the LAC value ranges obtained for potatoes,
mashua and oca tubers were similar. The total
antioxidant capacity of these crops is mainly attributed
to the phenolic compounds, which are present in
higher amounts than carotenoids.

CONCLUSIONS
This survey of Andean tuber germplasm for antioxidant compounds confirms that each type of crop
studied can be considered as an excellent source of
dietary phytochemicals (Fig. 5). The phytochemicals
responsible for the antioxidant capacity are related
to the phenolics and carotenoids present in each
tuber. The antioxidant values of these tuber crops
are higher than or comparable to known sources of
natural antioxidants, such as blueberries, indicating
that these crops have the potential to be considered
as important novel sources of nutraceuticals. These
Andean tuber crops hold great promise for producing
new and unique healthy, functional products for the
benefit of producers and consumers.

ACKNOWLEDGEMENTS
Carla Rios, Daniel Segura and Katherine Alejandro
are thanked for technical assistance.

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