Glucosinolate contents in maca ( Lepidium peruvianum Chacón) seeds, sprouts, mature plants and several derived commercial products

GLUCOSINOLATE CONTENTS IN MACA (LEPIDIUM PERUVIANUM CHACON) SEEDS, SPROUTS, MATURE PLANTS AND SEVERAL DERIVED COMMERCIAL PRODUCTS 1 GENYI LI , UWE AMMERMANN, AND CARLOS F. QUIROS Li, Genyi and Carlos F. Quir6s, (Department of Vegetable Crops, University of California, Davis, CA 95616), Uwe Arnmermann (Institute of Agronomy and Plant Breeding, University of Goettingen, von Siebold Str. 8, 37075 Goettingen, Germany). GLUCOSINOLATE CONTENT IN MACA (LEPIDIUM PERUVIANUM CHACON) SEEDS, SPROUTS, MATURE PLANTS AND SEVERAL DERIVED COMMERCIAL PRODUCTS. Economic Botany 55(2):255-262, 2001. Several products derived from processed maca hypocotyls (Lepidium pernvianum Chacdn, previously known as L. meyenii Walp.) were surveyed for glucosinolate content and quantified by HPLC analysis. These in- cluded pills, capsules, flour, liquor, tonic and mayonnaise. Different plant organs such as fresh hypocotyls and leaves, seeds, dry hypocotyls, and sprouts were also included in the survey. The most abundant glucosinolates detected in fresh and dry hypocotyls and leaves were the aromatic glucosinolates, benzylglucosinolate (glucotropaeolin) and p-methoxybenzylglucosinolate. Maca seeds and sprouts differed in profile from hypocotyls and leaves due to the modification of benzylglucosinolate. No glucosinolates were detected in liquor and tonic, while mayonnaise had only trace amounts of those glucosinolates. It had instead allylglucosinolate (sinigrin), which is an aliphatic glucosinolate. The pills, capsules and flour had the same glucosinolates as those observed in hypocotyls, but in variable amounts. The richest sources of glucosinolates were seeds, fresh hypocotyls and sprouts, in that order. CONTENIDO DE GLUCOSINOLATOS EN SEMILLAS DE MACA, PLANTULAS, PLANTAS MADURAS Y EN VARIOS PRODUCTOS DERIVADOS. Se determinaron glucosinolatos por HPLC (cromatograffa l{- quida de alto rendimiento) en la maca (Lepidium pernvianum Chac6n, antes L. meyenii Walp.) yen varios de sus productos derivados. Estos incluyeron comprimidos, cdpsulas, harina, licor, tonico y mayonesa de maca. Ademds de pldntulas, se muestrearon semillas, hojas e hipocotilos frescos, as{ como hipocotilos secos. Los glucosinolatos mds abundantes detectados en hojas y en hipocotilos frescos y secos fueron los aromdticos benzylglucosinolato (glucotropaeolin) y p-methoxybenzylglucosinolato. Las pldntulas y semillas mostraron perfiles de glucosinolatos diferentes al de las hojas e hipocotilos debido a la modificaci6n de benzylglucosinolato. No se detectaron glucosinolatos en el licor y tonico, mientras que el contenido de estos en la may- onesa fue mfnimo. Esta mds bien mostr6 el glucosinolato alifdtico allylglucosinolato (sinigrin). Los comprimidos, cdpsulas, y harina mostraron el mismo perfil de glucosinolatos que el de los hipocotilos. En orden de mayor a menor las fuentes mds ricas en glucosinolatos fueron las semillas, hipocotilos frescos y pldntulas. Key Words: Lepidium meyenii; nutraceuticals; anticarcinogens; secondary metabolism prod- ucts; Brassicaceae. Maca (Lepidium peruvianum Chac6n, previ- ously known as L. meyenii Walp.) is an Andean crop that belongs to the family Brassicaceae (Cruciferae) (Quiros and Aliaga 1997; Toledo et al. 1998; Thellung 1906). The genus Lepidium consists of approximately 175 species (Mum- menhoff et al. 1992), and is widely distributed ~Received 6 June 2000; accepted 16 November 2000. throughout the world in all continents except for Antarctica. The genus probably originates in the Mediterranean basin where most of the diploid species are found (Thellung 1906; Mummenhoff et al. 1992). Little is known about the time of origin of the genus and the mechanisms respon- sible for its worldwide distribution. Common ge- netic features observed in the immigrant species of Lepidium are autogamy and polyploidy (Qui- ros et al. 1996), which helped their establish- ment in new habitats. The Andean species of Economic Botany 55(2) pp. 255-262. 2001 �9 2001 by The New York Botanical Garden Press, Bronx, NY 10458-5126 U.S.A. 256 ECONOMIC BOTANY [VOL. 55 Lepidium are interesting because they grow at high-altitude habitats, up to 4500 m above sea level, and include several wild species besides the cultivated maca (Toledo et al. 1998). Prob- ably maca was domesticated in San Blas, Junin, between 1300 to 2000 years ago, but little is known about its origin (Rea 1992). Until very recently, maca was an Andean crop of narrow distribution, restricted to the Departments of Ju- n/n and Cerro de Pasco in the central Andes of Peru. It has one of the highest frost tolerances among native cultivated plants, since maca is able to grow in the puna, where only alpine grasses and bitter potatoes thrive (Castro de Le6n 1990; Le6n 1964; Tello et al. 1992). In 1994 less than 50 ha were being dedicated to the production of maca in Peru, and presum- ably in all the world (Tello et al. 1992; Mori and Huerta 1999). However, the recent popularity of maca as a medicinal crop has led the Ministry of Agriculture to instigate programs to increase production of maca and to expand its area of production to six other Departments of Peru. It is estimated that in 1999 1200 ha of maca were in production (Moil and Huerta 1999). This sud- den increase, often called the "maca boom," is due to increased demand for maca in Japan, Eu- rope and the U.S. This prompted the Peruvian government, in 1999, to prohibit exports of raw maca in an effort to curb its production in other countries, and to promote processing in Peru for the elaboration of added-value maca products such as pills, flour, drinks and other derivatives. The maca plant is a rosette of frilly leaves with an enlarged fleshy underground organ formed by the taproot and the lower part of the hypocotyl (Le6n 1964; Tello et al. 1992). These parts of the plant swell during growth, forming a storage organ resembling turnip (Brassica rapa L,) and radish (Raphanus sativus L.). Maca is cultivated for consumption of its root-hypo- cotyl axis, and is used extensively for medicinal purposes. According to folk belief, maca is an aphrodisiac, enhancing sexual drive and female fertility in humans and domestic animals. These attributes tend to be reduced at higher altitudes (Le6n 1964). Maca also is reported to increase energy and vitality (Rea 1992). Other medicinal properties attributed to maca include stress re- duction, regulation of hormonal secretion, stim- ulation of metabolism, memory improvement, antidepressant activity and effectiveness in com- bating anemia, leukemia, AIDS and cancer. Be- cause of these putative virtues, maca is also known by the name "Peruvian ginseng" (Rea 1992). Some of these attributes have been sub- stantiated by scientific research based on double- and triple-blind experiments on rats and human subjects. For example Aguilar et al. (1999) re- ported stress reduction in mice fed with diets supplemented with maca. The chemical com- position of maca supports the reputed medicinal benefits of maca as a food supplement. The nu- tritional value of the dried maca hypocotyl is high, resembling that found in cereal grains such as maize, rice and wheat. Fresh hypocotyls con- tain 80% water. Dry maca hypocotyls have the following composition: 59% carbohydrates, 10.2% proteins, 8.5% fiber, 2.2% lipids, and a few other compounds, including most of the es- sential amino acids (Dini et al. 1994), although apparently it lacks tryptophane (Repo-Carrasco 1999). Free fatty acids are also present in maca, of which linoleic, palmitic and oleic acids are the most abundant. Canales et al. (2000) ob- served higher growth rates in mice fed on diets supplemented with cooked maca hypocotyls, supporting the superior nutritional quality of this plant. Zheng et al. (2000) reported that maca contains novel polyunsaturated acids and their amides, called "macaene" and "macamide" by the authors. Maca also contains sterols, such as campesterol, stigmasterol and beta-sitosterol (Zheng et al. 2000) and is high in minerals, par- ticularly Fe, Ca and Cu. Alkaloids are also pre- sent, but these have yet to be characterized (Dini et al. 1994). Additionally, maca contains a high concentration of aromatic glucosinolates, benzyl and p-methoxybenzyl glucosinolate in particular, and their derived isothiocyanates (Johns 1981). These and their derived isothiocyanates are the compounds responsible for the pungent and pe- culiar flavor of maca, which is not palatable to many people. In most cases, its strong flavor is hidden by other components used in preparation of juices and other concoctions. Johns (1981) suggested that the fertility-enhancing properties of maca may be due to the presence of biolog- ically active aromatic isothiocyanates derived by hydrolysis of the glucosinolates, and specifically due to benzyl isothiocyanate and p-methoxyben- zyl isothiocyanates. The putative aphrodisiac powers of maca can be also attributed to the presence of prostaglandins and sterols in the hy- pocotyls (Dini et al. 1994) and to the amides of polyunsaturated fatty acids, which were presum- 2001] LI ET AL.: GLUCOSINOLATE CONTENTS IN MACA 257 ably found to enhance sexual function in rats and mice (Zheng et al. 2000). Most importantly, benzyl isothiocyanate has been reported to be a potent cancer inhibitor of mammary gland and stomach (Wattenberg 1981) and in liver (Sugie et al. 1992; Rosa et al. 1997) of rats treated with carcinogens. Today a large number of companies process and sell a myriad of maca products, such as soft drinks, liquor, flour, pills and capsules, tonic, mayonnaise and candies. The quality control of these companies ranges from strict sanitary and technical rules based on international standards to lax or non-existent controls. These products are sold in markets and drug stores in Peru and many of these products are exported abroad or are available for purchase through the World Wide Web as dietary supplements to increase stamina and fertility among other attributes. The objective of this paper is to report on a glucos- inolate survey on some of these products and compare it with the native profiles observed in different organs of the maca plant. MATERIALS AND METHODS PLANT MATERIAL Our survey included dried hypocotyls pur- chased at the local market in Junfn, Peru; fresh leaves and hypocotyls, and dried hypocotyls col- lected from mature maca plants (accession JTA192) grown at UC Davis in the winter of 1998. Dry maca seeds and sprouts at cotyledon stage from the same accession were also includ- ed in the study. The sprouts were produced by germinating seeds on paper towels in a plastic sandwich box for seven days. Samples from all these materials were frozen and stored at -80~ until the time of extraction. PROCESSED MATERIAL We sampled the following commercial prod- ucts sold and produced in Peru and advertised as maca hypocotyl derivatives: (1) 500 mg pills from two different producers: Cifarma, Lima "Macandina" (MA) and Productos Tropicales Naturistas, Lima (PN); (2) capsules from two different companies: Laboratory Cofana, Lima "New Millenium Maca" (NMM, 500 mg) and Laboratory Indoqufmica, Lima "Natural World Maca" (NW, 300 mg); (3) maca flour from the Universidad Nacional Agraria, La Molina, Lima; (4) liquor "Likor de Maca," Promaca, Huanca- yo; (5) "Maca Radish" mayonnaise from San Remo Restaurants, Lima; and (6) Reinforced Tonic of Maca from Inplame Natural, Lima. GLUCOSINOLATE ANALYSIS The analysis of glucosinolates followed the protocol by Kraling et al. (1990) with some modifications. For fresh root, leaf, and sprouts, 2g of tissue were frozen and ground in liquid nitrogen. After grinding, 3 ml of 70% hot meth- anol was added immediately and boiled at 75~ for 10 min, centrifuged at 3500 rpm, and the supernatant removed. Then another 3 ml of 70% methanol was added. The supernatant was mixed with the first extraction. For dry seeds, pills and dried hypocotyls, 1 g of each was ground into powder in a mortar and extracted twice as described above. For capsules, flour, mayonnaise, and liquor, 1 g of each was directly extracted twice with 70% methanol at 75~ for 10 min. 500txL of the extracts and the solution of glucosinolate standards sinigrin (Sigma) and glucotropaeolin (Sigma), were pipetted into an ion exchange column containing 20 mg Sephad- ex DEAE-A25 (Sigma), washed with 0.02M pyridine acetate buffer three times and with wa- ter twice. 100 txL of 0.5% sulfatase was added and kept for 16 h at room temperature. Desul- foglucosinolates were eluted with 1.5 ml water and analyzed using a Shimadzu HPLC, with c- 18 column at 229 nm wave length. The running program consisted of a linear gradient of 1%- 19% acetonitrile in water over 15 min, then con- stant elution at 19% acetonitrile for 10 min, and washing of the column with a linear gradient of 19%-100% acetonitrile for 20 min. The identi- fication of the glucosinolates was performed by using as standard the rapeseed variety "Linnet- ta" (Brassica napus L). Additionally, the glu- cosinolates, allyl glucosinolate (sinigrin) and benzyl glucosinolate (glucotropaeolin), were used as internal standards to confirm the identity of the peaks. The quantification was carried out by comparing the peak area of the samples with the mean peak area of the two standards. RESULTS AND DISCUSSION The main glucosinolates in fresh maca hypo- cotyls were the aromatic glucosinolates, benzyl glucosinolate (glucotropaoelin) and p-methoxy- benzyl glucosinolate (Fig. 1A), which is in agreement with the report of Johns (1981) for dried hypocotyls (Fig. 1B). We also identified several other glucosinolates such as 5-methyl- 258 ECONOMIC BOTANY [VOL. 55 A __A._.. . . . Jt .......... ,._.._ ............... _i 5.0 7.5 1o.o !i ,7.~ ,;.o . . . . . . . . . . 11.5 200 l lAi 2.~,~1 Itllll,tls B 2 J 1 D,0 i' 1 '~ i' 2~.~ 5 .0 12.5 15,0 t7.5 ~0.0 22.~ 25.0 C 40 . . . . . J t . . . . . . . . . . . . . . . . . -40 ~ o O0 2.5 50 }5 100 1s ~50 175 200 225 25~ MIn~te~ Fig. 1. HPLC profiles for maca hypocotyls and sprouts. Glucosinolates corresponding to major peaks: 1. Allyl glucosinolate, 2. 5-methylsulfinylpentyt glucosinolate, 3. p-hydroxybenzyl glucosinolate, 4. m-hydroxy- benzyl-glucosinolate (tentative identification), 5. Pent-4-enyl glucosinolate, 6. benzyt glucosinolate, 7. Indolyl- 3-methyl glucosinolate, 8. p-methoxybenzy lg lucos ino la te , 9. 4-methoxyindolyl-3-methyl glucosinolate. Glucos- inolates corresponding to the rest of the peaks were not identified. A. Fresh hypocotyls showing the highest glucosinolate concentration. B. Dry hypocotyl showing essentially the same profile as fresh hypocotyl but in lesser concentration. C. Sprouts. Note the change in the profile from benzyl glucosinolate (6) to (3) p-hydrox- ybenzyl glucosinolate. sulfinylpentyl glucosinolate (glucoalyssin), p-hydroxybenzyl glucosinolate (glucosinalbin), m-hydroxybenzyl glucosinolate (tentative iden- tification), Pent-4-enyl glucosinolate (glucobras- sicanapin) Indolyl-3-methyl glucosinolate (glu- cobrassicin) and 4-methoxyindolyl-3-methyl glucosinolate (4-methoxyglucobrassicin) (Fig. 1A, B, Table 1). In maca leaves, the glucosino- 2001] LIET AL.: GLUCOSINOLATE CONTENTS IN MACA 259 TABLE l. CONTENT OF GLUCOSINOLATES IN DIFFERENT MACA ORGANS AND PROCESSED PRODUCTS IN ~MOL]G (PERCENT OF EACH GLUCOSINOLATE*). (MA--CIFARMA, LIMA; PN--PRODUCTOS TROPICALES NATURISTAS, LIMA; NMM--LABORATORu COFANA, LIMA; NW--LABORATORu INDOQUfMICA, LIMA). Sample 1 2 3 4 5 6 7 8 9 Total Fresh hypocot 0.57 1.61 0.3 0.15 16.94 0.05 6.38 0.2 25.66 (2.2) (6.3) (0.2) (0.7) (66.4) (0.1) (25.0) (0.1) Fresh leaf 0.09 0.25 0.20 0.10 2.30 0.02 0.66 0.15 3.77 (2.4) (6.7) (5.3) (2.7) (60.5) (0.8) (17.6) (4.0) Seed 11.18 1.70 19.31 29.7 7.56 69.45 (16.0) (2.5) (28.0) (42.6) (10.8) Sprout 0.73 12.64 0.2 4.66 18.5 (3.9) (68.3) (1.1) (25.2) Dry hypocot 0.09 0.27 3.20 0.07 0.89 4.45 (1.8) (5.8) (71.0) (1.5) (20.0) Flour 0.05 0.49 2.70 0.88 4.06 (1.2) (12.1) (66.7) (21.7) Capsule (NMW) 0.11 0.50 3.78 1.35 1.01 6.67 (1.6) (7.5) (56.7) (20.2) (15.1) Capsule (NW) 0.05 0.27 1.78 0.47 2.57 (1.9) (10.5) (69.3) (18.3) Pill (PN) 0.13 0.71 6.10 1.32 8.25 (1.6) (8.6) (73.9) (16.0) Pill (MA) 0.1 0.41 2.31 0.58 3.40 (2.9) (12.1) (67.9) (17.1) Mayonnaise 2.14 0.48 0.07 2.69 (79.6) (17.8) (2.6) Liquor 0 Tonic 0 * 1. Allyl glucosinolate, 2. 5-methylsulfinylpentyl glucosinolate, 3. p-hydroxybenzyl glucosinolate, 4. m-hydroxybenzylglucosinolate (tentative iden- tification), 5. Pent-4-enyl glucosinolate, 6. benzyl glucosinolate, 7. Indolyl-3-methyl glucosinolate, 8. p-methoxybenzylglucosinolate, 9.4-methoxyin- dolyl-3-methyl glucosinolate, late profile was the same as that observed in fresh hypocotyls. The profile in maca seeds and sprouts differed from that of hypocotyls and leaves due the modification of benzyl glucosi- nolate. In seeds this compound was changed mainly to m-hydroxybenzyl glucosinolate, whereas in sprouts it was nearly completely changed into p-hydroxybenzyl glucosinolate or p-methoxybenzylglucosinolate (Fig. IC, Table 1). In the processed maca hypocotyl products tested, glucosinolate content was variable. The main glucosinolates in these products were ben- zyl glucosinolate and its modified derivatives (Fig. 2A, Table 1). In addition to these aromatic glucosinolates, some aliphatic types were also detected. In the dried hypocotyl from Peru, and in the flour, tab- lets and capsules, 5-methylsulfinylpentyl glucos- inolate was the predominant aliphatic glucosi- nolate, whereas in the mayonnaise, "Maca Rad- ish," it was allyl glucosinolate, which comprised nearly 80% of the total glucosinolates in this product (Fig. 2B, Table 1). This glucosinolate was not found in any other maca products or plant organs, so most likely it originates from an unknown additive used for the preparation of this product, such as mustard. In the liquor and tonic, another liquid product, no glucosinolates were detected by our analysis (Table 1). These were probably lost during dis- tillation. The quantities of glucosinolates varied considerably in each product and plant organ. The highest content of these compounds was ob- served in seeds, followed by fresh hypocotyls and then fresh sprouts (Table 1). The absolute content of glucosinolates in fresh maca hypocotyls is relatively higher than that reported in other crueiferous crops. It con- stituted approximately 1% of the fresh matter of the hypocotyl (assuming glucosinolate MW = 447), which is about 100 times more than that in Brassica oleracea leaves or inflorescences of 260 ECONOMIC BOTANY [VOL. 55 A 2 ; ,'o 1~ 2 'o 2's ~o Mlnutel B 4O 4O t 2o ,0 ! 6 / o ,.,. j~ ~_.....j, ~- - - -~ k_..._. J~ . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0 0.0 215 5.'0 . . . . 7:5 " 10'.0 12'.5 15'.0 17'.5 20' .0 "22',5 25.0 Mlnull* Fig. 2. HPLC profiles for two products derived from maca hypocotyl. A. Pills (PN) showing essentially the same hypocotyl glucosinolate profile. B. Mayonnaise containing allyl glucosinolate (1) and small amounts of benzyl glucosinolate (6) and p-methoxybenzylglucosinolate (8) characteristic of maca hypocotyls. its crops such as cabbage, cauliflower and broc- coli (Rosa et al. 1997). On the other hand, glu- cosinolate content in maca sprouts was compa- rable to that reported for broccoli sprouts by Fahey et al. (1997). Dried maca hypocotyls and their derived products had a much lower glu- cosinolate content than fresh tissue and seeds. The reason for this is that glucosinolates can be easily broken down into isothiocyanates during processing, especially if it involves breaking the tissue, which releases the enzyme involved in glucosinolate hydrolysis. Furthermore hydrox- ylated glucosinolate upon hydrolysis will pro- duce unstable isothiocyanates that will cyclize immediately into non-volatile oxalidine-2-thi- ones (Ettlinger and Kjaer 1968). Our results suggest that if the goal of a pro- cessing company is to produce products with high glucosinolate content, raw plant material is a better source for these compounds than dried material. For example, the higher content of glu- cosinolates in the pills from Productos Tropi- cales (PN) is explained by the use of raw hy- pocotyls, which are dehydrated at 70~ for 5 hours before going to the mill (Santos Jaimes, personal communication). Other products, such as flour, are based on cooked hypocotyls, which results in the loss and breakdown of a high pro- portion of glucosinolates (Rosa et al. 1997). We did not have information on processing proce- dures for the other products. In any case, the wide variation in glucosinolate content in pills and capsules from different companies could be due not only to different processing modalities, but also due to different amounts of actual plant material used in their manufacture. It is clear that all these products are genuine, since they contain the expected glucosinolates typical of maca. However, it is questionable whether there is any health benefit from consumption of maca liquor, tonic or mayonnaise. Isothiocyanate anal- ysis will be necessary to determine whether these products contain significant amounts of maca in their composition. 2001] LI ET AL.: GLUCOSINOLATE CONTENTS IN MACA 261 Additionally, our survey indicates that other plant parts and organs could also be used as a source of glucosinolates and their derived iso- thiocyanates. For example, leaves, which are normally discarded by the growers, could be used for processing. Seeds and sprouts could be commercialized as supplements, for consump- tion with other foods. Glucosinolates are just some of the products in maca that might have biological activity, translating into desirable medical and nutritional attributes. These derive cancer-protecting iso- thiocyanates by hydrolysis mediated by the en- zyme myrosinase, which is typically present in cruciferous plants as well as in the gut microflo- ra of mammals (Farnham et al. 2000). Testing for specific glucosinolates in maca serves not only to tell us whether a derivative product is authentic, but also to determine concentration levels of potentially cancer-protecting agents, which is very important for clients seeking this attribute. Although we only analyzed glucosi- nolate content in the present study, it would also be desirable to test for specific alkaloids and ste- rols if they prove to have the beneficial biolog- ical activity we currently suspect. ACKNOWLEDGMENTS We are indebted to Dr. Miguel Holle and Dr. Jose Aguilar for critical reading of the manuscript and for supplying some of the products tested in the study, to Ms. Karen OIson for editorial assistance and to Dr. Steffen Abel for generous access to his HPLC instrument. We are also indebted to Dr. Darush Struss for facilitating preliminary glucosinolate analysis and internal standards. LITERATURE CITED Aguilar, J. 1999. 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