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(Tropaeolum Tuberosum Ruíz & Pavón) in the Cuzco Region of Peru1

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(Tropaeolum Tuberosum Ruíz & Pavón) in the Cuzco Region of Peru1 29776_Ortega.qxd 4/14/06 2:27 PM Page 1 Glucosinolate Survey of Cultivated and Feral Mashua (Tropaeolum tuberosum Ruíz & Pavón) in the Cuzco Region of Peru1 Oscar R. Ortega, Dan Kliebenstein, Carlos Arbizu, Ramiro Ortega, and Carlos F. Quiros Oscar R. Ortega (Department of Plant Sciences, University of California, Davis, CA 95616; Centro Regional de Investigación en Biodiversidad Andina—CRIBA, Universidad Nacional San Antonio Abad del Cusco, Peru), Dan Kliebenstein (Department of Plant Sciences, Uni- versity of California, Davis, CA 95616), Carlos Arbizu (International Potato Center, POB 1558, Lima 12, Peru), Ramiro Ortega (Centro Regional de Investigación en Biodiversidad An- dina—CRIBA, Universidad Nacional San Antonio Abad del Cusco, Peru), and Carlos F. Quiros (Corresponding author, Department of Plant Sciences, University of California, Davis, CA 95616, e-mail: [email protected]). Glucosinolate Survey of Cultivated and Feral Mashua (Tropaeolum tuberosum Ruíz & Pavón) in the Cuzco Region of Peru. Economic Botany xx):xxx–xxx, 2006. Glucosinolates (GSL) present in cultivated and feral accessions of mashua (Tropaeolum tuberosum Ruíz & Pavón) were identified and quan- tified by High Performance Liquid Chromatography (HPLC) analysis. The main glucosino- lates detected were aromatic: 4–Hydroxybenzyl GSL (OHB, Glucosinalbin), Benzyl GSL (B, Glucotropaeolin), and m–Methoxybenzyl GSL (MOB, Glucolimnathin). The total amount of GSL observed ranged from 0.27 to 50.74 micromols per gram (␮Mol/g) of dried tuber tissue. Most of the low-content GSL accessions are distributed within the cultivated population with a total GSL concentration lower than 5.00 ␮Mol/g of dried tuber tissue. The highest total and specific GSL (OHB, B, and MOB) contents (more than 25.00 ␮Mol/g of dried tuber tissue) were observed in the feral population with few exceptions. In addition, only six different GSL profiles were found: Only MOB; only B; OHB and B; OHB and MO; B and MOB; and OHB, B and MOB. Se identificó y cuantificó mediante “High Performance Liquid Chromatograph” los glucosi- nolatos (GSL) presentes en mashua cultivada (Tropaeolum tuberosum Ruíz & Pavón) y sus parientes silvestres. Los compuestos principales descubiertos fueron los siguentes glucosino- latos aromáticos: 4–Hydroxybenzyl GSL (OHB, Glucosinalbin), Benzyl GSL (B, Glucotropae- olin) y m–Methoxybenzyl GSL (MOB, Glucolimnathin). El contenido total de GSL fluctuó entre 0.27 a 50.74 ␮Mol/g de tejido del tubérculo seco. La mayoría de las accesiones con bajo contenido de GSL estuvieron distribuidos dentro de la población cultivada con una con- centración total de GSL menor a 5.00 ␮Mol/g de tejido del tubérculo seco, mientras que el mas alto contenido total (más de 25.00 ␮Mol/g de tejido del tubérculo seco) y la mas alta concentración de GSL individuales (OHB, B y MOB) se observó en la población silvestre con pocas excepciones. Además, seis fenotipos de GSL diferentes fueron determinados: Sólo MOB; sólo B; OHB y B; OHB y MO; B y MOB; y OHB, B y MOB. Key words: Tropaeolum tuberosum; mashua; glucosinolate; benzyl; methoxybenzyl; anti- carcinogens; secondary metabolites; Andean tuber crops; isothiocyanates; glucotropaeolin. Glucosinolates (GSL) are secondary metabo- al. 2002, Robbelen et al. 1989). When plant tis- lites found in several families of dicotyledonous sue is disturbed by crushing, cutting, or other angiosperms, including the Brassicaceae and a physical damage, GSLs are brought into contact large number of other edible species (Wang et with the enzyme myrosinase (thioglucoside glu- cohydrolase), which rapidly hydrolyzes them. 1 Received 29 August 2005; accepted on 17 Febru- This hydrolysis yields unstable intermediates –s ary 2006. that, as dictated by chemical conditions as well –o –l Economic Botany, 60(2), 2006, pp. 000–000. © 2006, by The New York Botanical Garden Press, Bronx, NY 10458-5126 U.S.A. 29776_Ortega.qxd 4/14/06 2:27 PM Page 2 2 ECONOMIC BOTANY [VOL. 60 as by the presence of various accessory proteins, to by these authors as T. tuberosum ssp. sil- spontaneously release a variety of aglycone de- vestre. Mashua produces p–methoxybenzyl rivatives, such as isothiocyanates, thiocyanates, isothiocyanate, which gives mashua its charac- nitriles, oxazolidine–2–thiones (Wang et al. teristic piquant flavor, whereas the wild mate- 2002, Mithen 2001, Halkier 1999), and ep- rial is characterized by benzyl isothiocyanate, ithionitriles (Lambrix et al. 2001) plus elemen- 2–propyl isothiocyanate, and 2–butyl isothio- tary sulfur, depending on the concentration of cyanate (Johns and Towers 1981). In particular, H+ and other factors (Bones and Rossiter 1996). Benzyl isothiocyanate, which seems to be the Mashua (Tropaeolum tuberosum Ruíz & main isothiocyanate of mashua, is also found in Pavón spp. tuberosum) is a member of the fam- Nasturtium Tropaeolum majus (Lykkesfeldt and ily Tropaeolaceae (the Nasturtium familly) Møller 1993, Wielanek 1999). This compound (Sparre 1973, Sparre and Anderson 1991, Ruíz has been reported as a potent chemo-protective and Pavón 1802). It is also known as isañu (Ay- agent that blocks chemically induced carcino- mara-Bolivia), cubio (Colombia), añu, and genesis and prevents several types of cancer in ysaño, (Quechua in Peru and Bolivia) (Grau et rodents (Halkier and Du 1997, Stoner and al. 2000, Hernandez and León 1994, Herrera Morse 1997, Sugie et al. 1994, Wattenberg 1941). It ranks fourth in importance in the An- 1987 and 1992), including liver tumors (Sugie dean region after potato, oca, and ulluco (Na- et al. 1994, Rosa et al. 1997). Isothiocyanates tional Research Council [NRC] 1989); how- cause carcinogen detoxification prior to induc- ever, mashua is the least popular tuber crop tion of carcinogenesis and act as suppressing because of its bitterness due to the presence of agents to inhibit the neoplastic effects of car- isothiocyanates released by GSL hydrolysis cinogens, possibly by inducing apoptosis of (Johns and Towers 1981, Kjær et al. 1978). pre-cancerous cells or by adjusting key en- Isothiocyanates are well known for their biolog- zymes to reduce exposure of tissues to DNA ical activity as diuretics, as agents that can offer damage (Shapiro et al. 1998, Stoner and Morse protection against cancer, and as antibiotics, in- 1997). In addition, some recent studies of this secticides, and nematocides (Halkier and Du Andean crop done by Ramallo et al. (2004) 1997, Stoner and Morse 1997, Sugie et al. confirm the presence of p–methoxybenzyl GSL 1994, Wattenberg 1987 and 1992). These re- in six varieties of mashua from Bolivia. ports corroborate the extensive use of mashua The main objective of this paper is to deter- in Andean folk medicine to treat kidney ali- mine the GSL content of mashua cultivars ments, skin ulcers, kidney stones, and to kill grown in the Cusco region of Peru, of wild parasites. In addition, mashua is often used by forms of mashua collected in the same region, Andean growers as a pest repelling plant in bor- and a sample of cultivated mashua from the der rows surrounding potato fields because of germplasm collection maintained at the Interna- its putative fungicidal, bactericidal, nematoci- tional Potato Center (CIP). This sample is a dal, and allelopathic properties. These proper- good representation of the genetic variability of ties are probably conferred by its isothio- the species T. tuberosum. Such information will cyanates (Brabban and Edwards 1995, Johns et be useful for (1) future selection of genotypes al. 1982, NRC 1989). Two different kinds of with high content of beneficial GSL that could GSLs are found in the family Tropaeolaceae; be used as a source of functional foods or medi- (1) aliphatics derived from methionine, cine and (2) selection of low content GSL isoleucine, and valine and (2) aromatics derived mashua, thus removing the bitterness produced from phenylalanine and tyrosine (Fahey et al. by some of these compounds, to produce lines 2001). As reported by Johns (1981), mashua re- with improved palatability thus helping increase leases benzyl and p–methoxybenzyl isothio- the acceptability of this high protein crop. cyanates, derived from aromatic benzyl (B) and p–methoxybenzyl (MOB) GSL, respectively. Materials and Methods Indeed, additional phytochemical analyses of isothiocyanates by Kjær et al. (1978) and Johns Plant Material and Towers (1981) support the recognition of In June 2002, mashua tubers were harvested s– two subspecies in T. tuberosum: cultivated in the following communities of the Cuzco re- o– mashua and a tuber-bearing wild form, referred gion of Peru: (1) Matinga, Picol, and Qquecca- l– 29776_Ortega.qxd 4/14/06 2:27 PM Page 3 2006] ORTEGA, O. R., ET AL.: MASHUA GLUCOSINOLATES 3 yoc (Zone 1 located on the District of Taray in HPLC Analysis the Province of Calca) and (2) Ch’umpe, Po- From the resulting mixture (1.5 ml), 5 micro- q’ues, and Sayllafaya (Zone 2 located on the liters (␮l) were injected and separated using a District of Lamay in the Province of Calca). Agilent 1100 HPLC (High Performance Liquid Five mature and healthy mashua tubers per ac- Chromatograph) equipped with a Diode Array cession were sampled for each of the following Detector set at a wave length of 229 nanometers locations: 20 accessions from Matinga, 17 from (nm) for detection, using a RP–18 column (X Picol, two from Qqueccayoc (District of Taray- Terra) and a linear solvent gradient from 1% to Cusco–Peru); 57 from Ch’umpe, 92 from Po- 15% acetonitrile in water over 4 min, and wash- q’ues, 152 from Sayllafaya (district of Lamay- ing of the column with a linear gradient of 15% Cusco–Peru); 102 from the cultivated mashua to 95% acetonitrile for 6 minutes. The flow rate collection held by CIP (Peru); and 39 feral ac- was set at 0.9 ml/min, with a stop time of 8.5 cessions from different provinces of Cuzco min and a post time of 1.5 min, at 32°C.
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