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Comparative non-targeted metabolomics reveals differentiation of biochemical pathway network among fruits of natural populations and Cv. Alphonso of mango (Mangifera indica L.)

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Abstract

The focus of the metabolomic studies of mango fruit (Mangifera indica L.) so far has been mostly towards flavor and pulp quality metabolites and their biogenesis in domesticated cultivars. These studies are reliant on techniques, viz., gas chromatography and headspace solid-phase micro-extraction, and recently liquid chromatography–mass spectrometry. Here, we performed comparative untargeted metabolite analysis to understand flavor differentiation as fruit-specific changes in various biochemical pathways among Cv. Alphonso and two different natural mango populations from the Western Ghats, India. Significant stage-specific metabolome variations among these fruit sets were identified through principal component analysis. Furthermore, the multivariate analysis suggested quantitative expression variance in housekeeping and specialized metabolic pathways from the natural populations and Alphonso through network map for all the predominant biochemical pathways. The metabolites found in this study might be involved in growth and development processes, flavour, shelf-life, species interaction, and defences correlating with important general functions previously reported from mango and other fruits.

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Abbreviations

LC–MS:

Liquid chromatography–mass spectrometry

WG:

Western Ghats

EICs:

Extracted ion chromatograms

PCA:

Principal component analysis

BP:

Bhimashankar population

Cv.:

Cultivar

AUR:

Alphonso unripened

AR:

Alphonso ripened

BP1-UR:

Bhimashankar population-1 unripened

BP1-R:

Bhimashankar population-1 ripened

BP2-UR:

Bhimashankar population-2 unripened

BP2-R:

Bhimashankar population-2 ripened

UHPLC:

Ultra-high-performance liquid chromatography

References

  • Asfaw N, Demissew S (1994) Phytochemical dictionary: a handbook of bioactive compounds from plants. Econ Bot 48(3):258–258

    Article  Google Scholar 

  • Assaf H, Nafady A, Allam A, Hamed A, Kamel M (2020) Phytochemistry and biological activity of family "Urticaceae": a review (1957–2019). J Adv Biom Pharm Sci 3(3):150–176

    Google Scholar 

  • Beauvoit B, Belouah I, Bertin N, Cakpo CB, Colombié S, Dai Z, Gautier H, Génard M, Mo A (2018) Putting primary metabolism into perspective to obtain better fruits. Ann Bot 122:1–21

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bompard JM (2009) Chapter 2 Taxonomy and Systematics, the mango: botany, production and uses. CABI Wallingford, Cambridge, pp 19–36

    Book  Google Scholar 

  • Castro MD, Leyva AC, Vergaram CAC, Sanchez MAP, Flores SC, Flores AS, Kuhn DN, Osuna MAI (2015) Mango (Mangifera indica L.) Cv. Kent fruit mesocarp de novo transcriptome assembly identifies gene families important for ripening. Front Plant Sci 6:62

    Google Scholar 

  • Chambers MC, Maclean B, Burke R, Amodei D, Ruderman DL, Neumann S, Gatto L, Fischer B, Pratt B, Egertson J, Hoff K, Kessner D, Tasman N, Shulman N, Frewen B, Baker TA, Brusniak MY, Paulse C, Creasy D, Flashner L, Kani K, Moulding C, Seymour SL, Nuwaysir LM, Lefebvre B, Kuhlmann F, Roark J, Rainer P, Detlev S, Hemenway T, Huhmer A, Langridge J, Connolly B, Chadick T, Holly K, Eckels J, Deutsch EW, Moritz RL, Katz JE, Agus DB, MacCoss M, Tabb DL, Mallick P (2012) A cross-platform toolkit for mass spectrometry and proteomics. Nat Biotechnol 30(10):918–920

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chong J, Soufan O, Li C, Caraus I, Li S, Bourque G, Wishart DS, Xia J (2018) MetaboAnalyst 4.0: towards more transparent and integrative metabolomics analysis. Nucleic Acids Res 46:486–494

    Article  CAS  Google Scholar 

  • Chong J, Wishart DS, Xia J (2019) Using MetaboAnalyst 4.0 for comprehensive and integrative metabolomics data analysis. Curr Protoc Bioinform 68:e86 (128 pages)

    Article  Google Scholar 

  • Dar SM, Dholakia BB, Shanmugam H, Gupta VS, Subramanian KS, Subramanian J, Giri AP (2020) Differential modulation in metabolites revealed with the improvement in the shelf-life of Alphonso fruits. Mol Biotechnol 62:508–520. https://doi.org/10.1007/s12033-020-00267-7

    Article  CAS  PubMed  Google Scholar 

  • Dar SM, Oak P, Chidley H, Deshpande A, Giri A, Gupta V (2016) Nutrient and flavor content of mango (Mangifera indica L.) cultivars: an appurtenance to the list of staple foods A2-preedy. In: Monique SJ, Simmonds Victor R (eds) Nutritional composition of fruit cultivars. Academic Press, San Diego, p 445

    Google Scholar 

  • Deshpande AB, Anamika K, Jha V, Chidley HG, Oak P, Kadoo NY, Giri AP, Gupta VS (2017) Transcriptional transitions in Alphonso mango (Mangifera indica L.) during fruit development and ripening explain its distinct aroma and shelf life characteristics. Sci Rep 7:8711

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Deshpande AB, Chidley HG, Oak PS, Pujari KH, Giri AP, Gupta VS (2016) Data on changes in the fatty acid composition during fruit development and ripening of three mango cultivars (Alphonso, Pairi and Kent) varying in lactone content. Data Brief 9:480

    Article  PubMed  PubMed Central  Google Scholar 

  • Ediriweera MK, Tennekoon KH, Samarakoon SR, Thabrew I, Dilip DE, Silva E (2016) A study of the potential anticancer activity of Mangifera zeylanica bark: evaluation of cytotoxic and apoptotic effects of the hexane extract and bioassay-guided fractionation to identify phytochemical constituents. Oncol Lett 11(2):1335–1344

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • FAOSTAT (2017). https://www.fao.org/faostat/en/#data/QC/visualize.

  • Haminiuk CWI, Maciel GM, Plata-Oviedo MSV, Peralta RM (2012) Phenolic compounds in fruits-an overview. Int J Food Sci Tech 47:2023–2044

    Article  CAS  Google Scholar 

  • Ibrahim SRM, Mohamed GA (2016) Naturally occurring naphthalenes: chemistry, biosynthesis, structural elucidation, and biological activities. Phytochem Rev 15:279–295

    Article  CAS  Google Scholar 

  • Idstein H, Schreier P (1985) Volatile constituents of Alphonso mango (Mangifera indica). Phytochemistry 24:2313–2316

    Article  CAS  Google Scholar 

  • Jadhav SJ, Sharma RP, Salunkhe DK (1981) Naturally occurring toxic alkaloids in foods. Crit Rev Toxicol 9(1):21–104

    Article  CAS  PubMed  Google Scholar 

  • Jha SN, Narsaiah K, Sharma AD, Singh M, Bansal S, Kumar R (2008) Quality parameters of mango and potential of non-destructive techniques for their measurement-a review. J Food Sci Tech Mys 47:1–14

    Google Scholar 

  • Jiao XZ, Xie P, Zu LS, Liang XT (2003) Study of stereoselective synthesis of (±)-neocnidilide. J Asian Nat Prod Res 5(3):165–169

    Article  CAS  PubMed  Google Scholar 

  • Knill T, Schuster J, Reichelt M, Gershenzon J, Binder S (2008) Arabidopsis branched-chain aminotransferase 3 functions in both amino acid and glucosinolate biosynthesis. Plant Physiol 146:1028–1039

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kortstee AJ, Appeldoorn NJG, Oortwijn MEP, Visser RGF (2007) Differences in regulation of carbohydrate metabolism during early fruit development between domesticated tomato and two wild relatives. Planta 226:929–939

    Article  CAS  PubMed  Google Scholar 

  • Kostermans AJGH, Bompard JM (1993) The mangoes, their botany, nomenclature, horticulture and utilisation. Academic Press, London

    Google Scholar 

  • Kuhn DN, Bally ISE, Dillon NL, Innes D, Groh AM, Rahaman J, Ophir R, CohenY, and Sherman A, (2017) Genetic map of mango: a tool for mango breeding. Front Plant Sci 8:577

    Article  PubMed  PubMed Central  Google Scholar 

  • Kulkarni RS, Chidley HG, Pujari HG, Giri AP, Gupta VS (2012) Geographic variation in the flavour volatiles of Alphonso mango. Food Chem 130:58

    Article  CAS  Google Scholar 

  • Kulma A, Szopa J (2007) Catecholamines are active compounds in plants. Plant Sci 172:433–440

    Article  CAS  Google Scholar 

  • Kumar R, Bohra A, Pandey AK, Pandey MK, Kumar A (2017) Metabolomics for plant improvement: status and prospects. Front Plant Sci 8:1302

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu M, Lu S (2016) Plastoquinone and ubiquinone in plants: biosynthesis, physiological function and metabolic engineering. Front Plant Sci 7:1898

    PubMed  PubMed Central  Google Scholar 

  • Ma XW, Wu HX, Liu LQ, Yao QS, Wang SB, Zhan RL (2011) Polyphenolic compounds and antioxidant properties in mango fruits. Sci Hortic 129:102

    Article  CAS  Google Scholar 

  • Metsalu T, Vilo J (2015) Clustvis: a web tool for visualizing clustering of multivariate data using principal component analysis and heatmap. Nucleic Acids Res 43(W1):W566–W570

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moss MO (2008) Fungi, quality and safety issues in fresh fruits and vegetables. J Appl Microbiol 104(5):1239–1243

    Article  CAS  PubMed  Google Scholar 

  • Ncube BSJV (2015) Tilting plant metabolism for improved metabolite biosynthesis and enhanced human benefit. Molecules 20(7):12698

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Noel JP, Austin MB, Bomati EK (2005) Structure–function relationships in plant phenylpropanoid biosynthesis. Curr Opin Plant Biol 8:249

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oak P, Deshpande A, Giri A, Gupta V (2019) Metabolomic dynamics reveals oxidative stress in spongy tissue disorder during ripening of Mangifera indica L. fruit. Metabolites 9(11):255

    Article  CAS  PubMed Central  Google Scholar 

  • Oikawa A, Otsuka T, Nakabayashi R, Jikumaru Y, Isuzugawa K, Murayama H, Saito K, Shiratake K (2015) Metabolic profiling of developing pear fruits reveals dynamic variation in primary and secondary metabolites, including plant hormones. PLoS ONE 10:1–18

    Google Scholar 

  • Pandit SS, Chidley HG, Kulkarni RS, Pujari KH, Giri AP, Gupta VS (2009a) Cultivar relationships in mango based on fruit volatile profiles. Food Chem 114:363

    Article  CAS  Google Scholar 

  • Pandit SS, Kulkarni RS, Chidley HG, Giri AP, Pujari KH, Kollner TG, Degenhardt J, Gershenzon J, Gupta VS (2009b) Changes in volatile composition during fruit development and ripening of ‘Alphonso’ mango. J Sci Food Agric 89:2071

    Article  CAS  Google Scholar 

  • Pang Z, Chong J, Li S, Xia J (2020) MetaboAnalystR 3.0: toward an optimized workflow for global metabolomics. Metabolites 10(5):186

    Article  CAS  PubMed Central  Google Scholar 

  • Peled-Zehavi H, Oliva M, Xie Q, Tzin V, Oren-Shamir M, Aharoni A, Galili G (2015) Metabolic engineering of the phenylpropanoid and its primary, precursor pathway to enhance the flavor of fruits and the aroma of flowers. Bioengineering 2(4):204–212

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pino JA, Mesa J, Munoz Y, Marti MP, Marbot R (2005) Volatile components from mango (Mangifera indica L.) cultivars. J Agric Food Chem 53:2213–2223

    Article  CAS  PubMed  Google Scholar 

  • Prasanna V, Prabha TN, Tharanathan RN (2007) Fruit ripening phenomena-an overview. Crit Rev Food Sci Nutr 47(1):1–19

    Article  CAS  PubMed  Google Scholar 

  • Rigano MM, Raiola A, Docimo T, Ruggieri V, Calafiore R, Vitaglione P, Ferracane R, Frusciante L, Barone A (2016) Metabolic and molecular changes of the phenylpropanoid pathway in tomato (Solanum lycopersicum) lines carrying different Solanum pennellii wild chromosomal regions. Front Plant Sci 7:1484

    Article  PubMed  PubMed Central  Google Scholar 

  • Salazar-Cerezo S, Martinez-Montiel N, Garcia-Sanchez J, Perez YTR, Martinez-Contreras RD (2018) Gibberellin biosynthesis and metabolism: a convergent route for plants, fungi and bacteria. Microbiol Res 208:85–98

    Article  CAS  PubMed  Google Scholar 

  • Serrani JC, Sanjuán R, Ruiz-Rivero O, Fos M, García-Martínez JL (2007) Gibberellin regulation of fruit set and growth in tomato. Plant Physiol 145:246–257

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh P, Russell GB, Hayashi Y, Gallagher RT, Fredericksen S (1979) The insecticidal activity of some norditerpene dilactones. Entomol Exp Appl 25:121–127

    Article  CAS  Google Scholar 

  • Smirnoff N (2001) L-ascorbic acid biosynthesis. Vitam Horm 61:241–266

    Article  CAS  PubMed  Google Scholar 

  • Sumner L, Amberg A, Barette D, Beale M, Beger R, Daykin C, Fan T, Fiehn O, Goodacre R, Groffin J, Hankemeier T, Hardy N, Harnly J (2007) Proposed minimum reporting standards for chemical analysis Chemical Analysis Working Group (CAWG) Metabolomics Standards Initiative (MSI). Metabolomics 3(3):211–221

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • U.S. Department of Agriculture, Agricultural Research Service (1992–2016) Dr. Duke's phytochemical and ethnobotanical databases. Home Page, https://phytochem.nal.usda.gov/

  • Valavi SG, Rajmohan K, Govil JN, Peter KV, Thottappilly G (2012) Mango, production and processing technology, 1st edn. Studium Press, Houston

    Google Scholar 

  • Veltman RH, Lentheric I, Van der Plas LHW, Peppelenbos HW (2003) Internal browning in pear fruit (Pyrus communis L. cv. Conference) may be a result of a limited availability of energy and antioxidants. Postharvest Biol Technol 28:295–302

    Article  CAS  Google Scholar 

  • Wang P, Luo Y, Huang J, Gao S, Zhu G, Dang Z, Gai J, Yang M, Zhu M, Zhang H, Ye X, Gao A, Tan X, Wang S, Wu S, Cahoon EB, Bai B, Zhao Z, Li Q, Wei J, Chen H, Luo R, Gong D, Tang K, Zhang B, Ni Z, Huang G, Hu S, Chen Y (2020) The genome evolution and domestication of tropical fruit mango. Genom Biol 21:60

    Article  CAS  Google Scholar 

  • Wannan BS (2006) Analysis of generic relationships in Anacardiaceae. Blumea Biodivers Evol Biogeogr Plants 5:31

    Google Scholar 

  • Warschefsky EJ, Von Wettberg EJB (2019) Population genomic analysis of mango (Mangifera indica) suggests a complex history of domestication. New Phytol 222:2023–2037

    Article  CAS  PubMed  Google Scholar 

  • Wiame E, Lamosa P, Santos H, Schaftingen EV (2005) Identification of glucoselysine-6-phosphate deglycase, an enzyme involved in the metabolism of the fructation product glucoselysine. Biochem J 392(2):263–269

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Winter G, Todd CD, Trovato M, Forlani G, Funck D (2015) Physiological implications of arginine metabolism in plants. Front Plant Sci 6:534

    Article  PubMed  PubMed Central  Google Scholar 

  • Wu BH, Turion BQ, Génard M, Li SH, Zhao JB, Yang J, Wang YQ (2012) Application of a SUGAR model to analyse sugar accumulation in peach cultivars that differ in glucose–fructose ratio. J Agric Sci 150:53–63

    Article  CAS  Google Scholar 

  • Xia J, Wishart DS (2011a) Web-based inference of biological patterns, functions and pathways from metabolomic data using MetaboAnalyst. Nat Protoc 6(6):743–760

    Article  CAS  PubMed  Google Scholar 

  • Xia J, Wishart DS (2011b) Metabolomic data processing, analysis, and interpretation using MetaboAnalyst. Curr Protoc Bioinform 14:1–48

    Google Scholar 

  • Xu J, Fang X, Li C, Yang L, Chen XY (2020) General and specialized tyrosine metabolism pathways in plants. aBIOTECH 1:97–105

    Article  Google Scholar 

  • Yannai S (2003) Dictionary of food compounds with CD-ROM. Chapman and Hall/CRC, New York

    Book  Google Scholar 

Download references

Acknowledgements

MSD is thankful to Council of Scientific and Industrial Research (CSIR, New Delhi) for research fellowship; to the Academy of Scientific and Innovative Research (AcSIR), India for enrolment in the Ph.D. program; and to Dr. Narendra Kadoo (CSIR-NCL) for help in generation of .mol file using the R-code. The authors acknowledge help from a farmer Mr. Kundalik Kondhawale from Mattrachi wadi, Bhimashankar forest area during sample collection. This research was funded by the CSIR, New Delhi, India under the project CSC0133 (FUNHEALTH) to CSIR-NCL, Pune.

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Authors and Affiliations

  1. Plant Molecular Biology Unit, Biochemical Sciences Division, CSIR-National Chemical Laboratory, Dr. Homi Bhabha Road, Pune, Maharashtra, 411008, India

    M. Saleem Dar, Yashwant Kumar, Vidya S. Gupta & Ashok P. Giri

  2. Academy of Scientific and Innovative Research (AcSIR), Ghaziabad, Uttar Pradesh, 201002, India

    M. Saleem Dar, Vidya S. Gupta & Ashok P. Giri

  3. Translational Health Science and Technology Institute (THSTI), Faridabad, Uttar Pradesh, 121001, India

    Yashwant Kumar

  4. Biospheres, Eshwari, 52/403, Lakshminagar, Parvati, Pune, Maharashtra, 411009, India

    Sachin A. Punekar

  5. Indian Institute of Science Education and Research, Pune, Maharashtra, 411008, India

    Bhushan B. Dholakia

  6. MBB Department, Tripura University, Suryamaninagar, 799022, India

    Bhushan B. Dholakia

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  1. M. Saleem Dar
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  4. Vidya S. Gupta
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  5. Bhushan B. Dholakia
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Contributions

APG, BBD, MSD, and YK conceptualized the idea, and subsequently, MSD carried out the experiments. MSD, SAP, BBD, and APG collected fruit samples. SAP identified the natural and cultivated mango populations and prepared the morphological and taxonomical interpretations. YK helped in method optimization for data acquisition and R-analysis-based Prometab code modification specific to our data set. Subsequently, MSD and YK prepared the figures and tables with suggestions from BBD, SAP, and APG. MSD wrote the initial draft of the manuscript with suggestions from YK, SAP, BBD, APG, and VSG. All authors contributed in revising and editing the manuscript drafts; and approved the final manuscript.

Corresponding authors

Correspondence to Bhushan B. Dholakia or Ashok P. Giri.

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Dar, M.S., Kumar, Y., Punekar, S.A. et al. Comparative non-targeted metabolomics reveals differentiation of biochemical pathway network among fruits of natural populations and Cv. Alphonso of mango (Mangifera indica L.). J Proteins Proteom 11, 269–282 (2020). https://doi.org/10.1007/s42485-020-00047-6

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