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Planta Med 2020; 86(10): 674-685
DOI: 10.1055/a-1161-0372
Natural Product Chemistry and Analytical Studies
Original Papers
Georg Thieme Verlag KG Stuttgart · New York

Characterization of Maca (Lepidium meyenii/Lepidium peruvianum) Using a Mass Spectral Fingerprinting, Metabolomic Analysis, and Genetic Sequencing Approach

Ping Geng
1   Methods and Application of Food Composition Lab, Beltsville Human Nutrition Research Center, Agriculture Research Service, US Department of Agriculture, Beltsville, MD, USA
,
Jianghao Sun
1   Methods and Application of Food Composition Lab, Beltsville Human Nutrition Research Center, Agriculture Research Service, US Department of Agriculture, Beltsville, MD, USA
,
Pei Chen
1   Methods and Application of Food Composition Lab, Beltsville Human Nutrition Research Center, Agriculture Research Service, US Department of Agriculture, Beltsville, MD, USA
,
Eric Brand
2   School of Chinese Medicine, Hong Kong Baptist University, Kowloon Tong, Hong Kong SAR
,
James Frame
3   Natural Health International, San Francisco, CA, USA
,
Henry Meissner
4   Faculty of Health Studies, Charles Sturt University & Therapeutic Research, TTD International Pty Ltd, Elanora, QLD, Australia
,
Jeremy Stewart
5   Gaia Herbs, Brevard, NC, USA
,
Stefan Gafner
6   American Botanical Council, Austin, TX, USA
,
Stephanie Clark
7   NSF International Authenticity Laboratory, Petaluma, CA, USA
,
Jesse Miller
7   NSF International Authenticity Laboratory, Petaluma, CA, USA
,
James Harnly
1   Methods and Application of Food Composition Lab, Beltsville Human Nutrition Research Center, Agriculture Research Service, US Department of Agriculture, Beltsville, MD, USA
› Author Affiliations
Further Information

Publication History

received 30 May 2019
revised 01 April 2020

accepted 19 April 2020

Publication Date:
20 May 2020 (online)

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Abstract

Maca (Lepidium meyenii, synonym L. peruvianum) was analyzed using a systematic approach employing principal component analysis of flow injection mass spectrometry fingerprints (no chromatographic separation) to guide the selection of samples for metabolite profiling and DNA next generation sequencing. Samples consisted of 39 commercial maca supplements from 11 manufacturers, 31 unprocessed maca tubers grown in Peru and China, and a historic non-tuber maca sample from Peru. Principal component analysis of flow injection mass spectrometry fingerprints initially placed all the maca samples in three classes with similar chemical composition: commercial maca samples, tubers grown in Peru, and tubers grown in China. Metabolite profiling identified 67 compounds in the negative mode and 51 compounds in the positive mode. Compounds identified by metabolite profiling (macamides, glucosinolates, amino acids, fatty acids, polyunsaturated fatty acids, saccharides, imidazoles) were then used to identify ions in the flow injection mass spectrometry fingerprints. The tuber fingerprints were analyzed by factorial multivariate analysis of variance revealing that black, red, and yellow maca from Peru and black and yellow maca from China were compositionally different with respect to color and country. Critical ions were identified that allowed for the differentiation of maca between colors from the same country or between two countries with the same color. Genetically, all samples were confirmed to be L. meyenii based on next generation sequencing at three gene regions (ITS2, psbA, and trnL) and comparison to recorded sequences of vouchered standards.

Key words

maca - Lepidium meyenii - Brassicaceae - flow injection mass spectrometry - metabolite profiling - imidazoles - macamides - glucosinolates - PCA

Supporting Information

    Sample description (Table 1S), compound identification (Tables 2S and 3S), chromatograms of tuber samples (Figs. 1S and 2S), and genetic sequences (Figs. 3S–5S) are available as Supporting Information.

  • Supporting Information
 

  • References

  • 1 Hermann M, Heller J. eds. Andean Roots and Tubers: Ahipa, Arracacha, Maca and Yacon. Rome, Italy: International Plant Genetics Research Institute; 1997: 175-194
    Google Scholar
  • 2 Balick MJ, Lee R. Maca: from traditional food crop to energy and libido stimulant. Altern Ther Health Med 2002; 8: 96
    PubMedGoogle Scholar
  • 3 Valerio LG, Gonzales GF. Toxicological aspects of the South American herbs catʼs claw (Uncaria tomentosa) and maca (Lepidium meyenii): a critical synopsis. Toxicol Rev 2005; 24: 11-35
    CrossrefPubMedGoogle Scholar
  • 4 Meissner HO, Mscisz A, Kedzia B, Pisulewski P, Piątkowska E. Peruvian Maca: Two scientific names Lepidium Meyenii Walpers and Lepidium Peruvianum Chacon – are they phytochemically-synonymous?. Int J Biomed Sci 2015; 11: 1-15
    PubMedGoogle Scholar
  • 5 Wang Y, Wang Y, McNeil B, Harvey LM. Maca: an Andean crop with multi-pharmacological functions. Food Res Int 2007; 40: 783-792
    CrossrefPubMedGoogle Scholar
  • 6 Zhang J, Wang HM, Zhao YL, Zuo ZT, Wang YZ, Jin H. Comparison of mineral element content in a functional food maca (Lepidium meyenii Walp.) from Asia and South America. J Anal Methods Chem 2015; 2015: 530541
    PubMedGoogle Scholar
  • 7 Wang S, Zhu F. Chemical composition and health effects of maca (Lepidium meyenii). Food Chem 2019; 288: 422-443
    CrossrefPubMedGoogle Scholar
  • 8 Dini A, Migliuolo G, Rastrelli L, Saturninoc P, Schettinoc O. Chemical composition of Lepidium meyenii . Food Chem 1994; 49: 347-349
    CrossrefPubMedGoogle Scholar
  • 9 Muhammad I, Zhao J, Dunbar DC, Khan IA. Constituents of Lepidium meyenii ‘maca’. Phytochemistry 2002; 59: 105-110
    CrossrefPubMedGoogle Scholar
  • 10 Cui B, Zheng BL, He K, Zheng QY. Imidazole alkaloids from Lepidium meyenii . J Nat Prod 2003; 66: 1101-1103
    CrossrefPubMedGoogle Scholar
  • 11 Jin W, Chen X, Dai P, Yu L. Lepidiline C and D: two new imidazole alkaloids from Lepidium meyenii Walpers (Brassicaceae) roots. Phytochem Lett 2016; 17: 158-161
    CrossrefPubMedGoogle Scholar
  • 12 Yu MY, Qin XJ, Peng XR, Yu L. Macathiohydantoins B–K, novel thiohydantoin derivatives from Lepidium meyenii . Tetrahedron 2017; 73: 4392-4397
    CrossrefPubMedGoogle Scholar
  • 13 Yu MY, Qin XJ, Shao LD, Peng X, Li L, Yang H, Qiu MH. Macahydantoins A and B, two new thiohydantoin derivatives from Maca (Lepidium meyenii): structural elucidation and concise synthesis of macahydantoin A. Tetrahedron Lett 2017; 58: 1684-1686
    CrossrefPubMedGoogle Scholar
  • 14 Tian X, Peng X, Yu M, Huang Y, Wang X, Zhou L, Qiu MH. Hydantoin and thioamide analogues from Lepidium meyenii . Phytochem Lett 2018; 25: 70-73
    CrossrefPubMedGoogle Scholar
  • 15 Zhou M, Ma HY, Liu ZH Yang GY, Du G, Ye YQ, Li GP, Hu QF. (+)-Meyeniins A–C, novel hexahydroimidazo[1,5-c]thiazole derivatives from the tubers of Lepidium meyenii: complete structural elucidation by biomimetic synthesis and racemic crystallization. J Agric Food Chem 2017; 65: 1887-1892
    CrossrefPubMedGoogle Scholar
  • 16 Zhao J, Muhammad I, Dunbar DC, Mustafa J, Khan IA. New alkamides from maca (Lepidium meyenii). J Agric Food Chem 2005; 53: 690-693
    CrossrefPubMedGoogle Scholar
  • 17 Xia C, Chen J, Deng JL, Zhu YQ, Li WY, Jie B, Chen TY. Novel macamides from maca (Lepidium meyenii Walpers) root and their cytotoxicity. Phytochem Lett 2018; 25: 65-69
    CrossrefPubMedGoogle Scholar
  • 18 Piacente S, Carbone V, Plaza A, Zampelli A, Pizza C. Investigation of the tuber constituents of maca (Lepidium meyenii Walp.). J Agric Food Chem 2002; 50: 5621-5625
    CrossrefPubMedGoogle Scholar
  • 19 Yábar E, Pedreschi R, Chirinos R, Campos D. Glucosinolate content and myrosinase activity evolution in three maca (Lepidium meyenii Walp.) ecotypes during preharvest, harvest and postharvest drying. Food Chem 2011; 127: 1576-1583
    CrossrefPubMedGoogle Scholar
  • 20 Zhou M, Zhang RQ, Chen YJ, Liao LM, Sun YQ, Ma ZH, Yang QF, Li P, Ye YQ, Hu QF. Three new pyrrole alkaloids from the roots of Lepidium meyenii . Phytochem Lett 2018; 23: 137-140
    CrossrefPubMedGoogle Scholar
  • 21 Clement C, Diaz Grados DA, Avula B, Khan IA, Mayer AC, Ponce Aguirre DD, Manrique I, Kreuzer M. Influence of colour type and previous cultivation on secondary metabolites in hypocotyls and leaves of maca (Lepidium meyenii Walpers). J Sci Food Agric 2010; 90: 861-869
    CrossrefPubMedGoogle Scholar
  • 22 Beharry S, Heinrich M. Is the hype around the reproductive health claims of maca (Lepidium meyenii Walp.) justified?. J Ethnopharmacol 2018; 211: 126-170
    CrossrefPubMedGoogle Scholar
  • 23 Zhao J, Avula B, Chan M, Clément C, Kreuzer M, Khan IA. Metabolomic differentiation of maca (Lepidium meyenii) accessions cultivated under different conditions using NMR and chemometric analysis. Planta Med 2012; 78: 90-101
    Article in Thieme ConnectPubMedGoogle Scholar
  • 24 Meissner HO, Mscisz A, Baraniak M, Piatkowska E, Pisulewski P, Mrozikiewicz M, Bobkiewicz-Kozlowska T. Peruvian Maca (Lepidium peruvianum) – III: The effects of cultivation altitude on phytochemical and genetic differences in the four prime maca phenotypes. Int J Biomed Sci 2017; 13: 58-73
    PubMedGoogle Scholar
  • 25 Clement C, Diaz D, Manrique I, Avula B, Khan IA, Ponce Aguirre DD, Kunz C, Mayer AC, Kreuzer M. Secondary metabolites in maca as affected by hypocotyl color, cultivation history, and site. Agron J 2010; 102: 431-439
    CrossrefPubMedGoogle Scholar
  • 26 Melnikovova I, Havlik J, Fernandez Cusimamani E, Milella L. Macamides and fatty acids content comparison in maca cultivated plant under field conditions and greenhouse. Bol Latinoam Caribe Plant Med Aromat 2012; 11: 420-427
    PubMedGoogle Scholar
  • 27 Chen L, Li J, Fan L. The nutritional composition of maca in hypocotyls (Lepidium meyenii Walp.) cultivated in different regions of china. J Food Qual 2017; 2017: 8
    PubMedGoogle Scholar
  • 28 Pan Y, Zhang J, Li H, Wang YZ, Li WY. Characteristic fingerprinting based on macamides for discrimination of maca (Lepidium meyenii) by LC/MS/MS and multivariate statistical analysis. J Sci Food Agric 2016; 96: 4475-4483
    CrossrefPubMedGoogle Scholar
  • 29 Hollingsworth PM, Forrest LL, Spouge JL, Hajibabaei M, Ratnasingham S, van der Bank M, Chase MW, Cowan RS, Erickson DL, Fazekas AJ, Graham SW, James KE, Kim KJ, Kress WJ, Schneider H, van AlphenStahl J, Barrett SC, van den Berg C, Bogarin D, Burgess KS, Cameron KM, Carine M, Chacón J, Clark A, Clarkson JJ, Conrad F, Devey DS, Ford CS, Hedderson TA, Hollingsworth ML, Husband BC, Kelly LJ, Kesanakurti PR, Kim JS, Kim YD, Lahaye R, Lee HL, Long DG, Madriñán S, Maurin O, Meusnier I, Newmaster SG, Park CW, Percy DM, Petersen G, Richardson JE, Salazar GA, Savolainen V, Seberg O, Wilkinson MJ, Yi DK, Little DP. A DNA barcode for land plants. Proc Natl Acad Sci U S A 2009; 106: 12794-12797
    CrossrefPubMedGoogle Scholar
  • 30 Meissner HO, Mscisz A, Mrozikiewicz M, Baraniak M, Mielcarek S, Kedzia B, Piatkowska E, Jólkowska J, Pisulewski P. Peruvian maca (Lepidium peruvianum): (I) phytochemical and genetic differences in three maca phenotypes. Int J Biomed Sci 2015; 11: 131-145
    PubMedGoogle Scholar
  • 31 Hall RD. Plant metabolomics: from holistic hope, to hype, to hot topic. New Phytol 2006; 169: 453-468
    CrossrefPubMedGoogle Scholar
  • 32 Brereton RG. Chemometrics for Pattern Recognition. West Sussex, U.K: John Wiley & Sons; 2009
    Google Scholar
  • 33 Zhu ZJ, Schultz AW, Wang J, Johnson CH, Yannone SM, Patti GJ, Siuzdak G. Liquid chromatography quadrupole time-of-flight mass spectrometry characterization of metabolites guided by the METLIN database. Nat Protoc 2013; 8: 451
    CrossrefPubMedGoogle Scholar
  • 34 Pan Y, Zhang J, Li H, Wang Y, Li WY. Simultaneous analysis of macamides in maca (Lepidium meyenii) with different drying process by liquid chromatography tandem mass spectrometry. Food Anal Methods 2016; 9: 1686-1695
    CrossrefPubMedGoogle Scholar
  • 35 Geng P, Zhang M, Harnly J, Luthria DL, Chen P. Use of fuzzy chromatography mass spectrometric (FCMS) fingerprinting and chemometric analysis for differentiation of whole-grain and refined wheat (T. aestivum) flour. Anal Bioanal Chem 2015; 407: 7875-7888
    CrossrefPubMedGoogle Scholar
  • 36 Geng P, Sun J, Zhang M, Li X, Harnly JM, Chen P. Comprehensive characterization of C-glycosyl flavones in wheat (Triticum aestivum L.) germ using UPLC-PDA-ESI/HRMSn and mass defect filtering. J Mass Spectrom 2016; 51: 914-930
    CrossrefPubMedGoogle Scholar
  • 37 Sun J, Chen P. A flow-injection mass spectrometry fingerprinting method for authentication and quality assessment of Scutellaria lateriflora-based dietary supplements. Anal Bioanal Chem 2011; 401: 1577-1584
    CrossrefPubMedGoogle Scholar
  • 38 Geng P, Harnly JM, Chen P. Differentiation of whole grain from refined wheat (T. aestivum) flour using lipid profile of wheat bran, germ, and endosperm with UHPLC-HRAM mass spectrometry. J Agric Food Chem 2015; 63: 6189-6211
    CrossrefPubMedGoogle Scholar
  • 39 Holman JD, Tabb DL, Mallick P. Employing ProteoWizard to convert raw mass spectrometry data. Curr Protoc Bioinformatics 2014; 46: 13.24.1-13.24.9
    PubMedGoogle Scholar
  • 40 Luthria DL, Lin LZ, Robbins RJ, Finley JW, Banuelos GS, Harnly JM. Discriminating between cultivars and treatments of broccoli using mass spectral fingerprinting and analysis of variance-principal component analysis. J Agric Food Chem 2008; 56: 9819-9827
    CrossrefPubMedGoogle Scholar
  • 41 Luthria DL, Mukhopadhyay S, Robbins RJ, Finley JW, Banuelos GS, Harnly JM. UV spectral fingerprinting and analysis of variance-principal component analysis: a useful tool for characterizing sources of variance in plant materials. J Agric Food Chem 2008; 56: 5457-5462
    CrossrefPubMedGoogle Scholar
  • 42 Harnly JM, Pastor-Corrales MA, Luthria DL. Variance in the chemical composition of dry beans determined from UV spectral fingerprints. J Agric Food Chem 2009; 57: 8705-8710
    CrossrefPubMedGoogle Scholar
  • 43 Doyle J, Doyle J. A rapid procedure for DNA purification from small quantities of fresh leaf tissue. Phytochem Bull 1987; 19: 11-15
    PubMedGoogle Scholar
  • 44 Taberlet P, Gielly L, Pautou G, Bouvet J. Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Mol Biol 1991; 17: 1105-1109
    CrossrefPubMedGoogle Scholar
  • 45 Chen S, Yao H, Han J, Liu C, Song J, Shi L, Zhu Y, Ma X, Gao T, Pang X, Luo K, Li Y, Li X, Jia X, Lin Y, Leon C. Validation of the ITS2 region as a novel DNA barcode for identifying medicinal plant species. PLoS One 2010; 5: e8613
    CrossrefPubMedGoogle Scholar