1932

Abstract

Plants produce a diversity of plant secondary metabolites (PSMs), which function as defense chemicals against herbivores and microorganisms but also as signal compounds. An individual plant produces and accumulates mixtures of PSMs with different structural features using different biosynthetic pathways. Almost all PSMs exert one or several biological activities that can be useful for nutrition and health. This review discusses the modes of action of PSMs alone and in combinations. In a mixture, most individual PSMs can modulate different molecular targets; they are thus multitarget drugs. In an extract with many multitarget chemicals, additive and synergistic effects occur. Experiments with the model system show that polyphenols and carotenoids can function as powerful antioxidative and longevity-promoting PSMs. PSMs of food plants and spices often exhibit antioxidant, anti-inflammatory, and antimicrobial properties, which can be beneficial for health and the prevention of diseases. Some extracts from food plants and spices with bioactive PSMs have potential for nutraceuticals and antimicrobials.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-food-052720-100326
2022-03-25
2024-06-15
Loading full text...

Full text loading...

/deliver/fulltext/food/13/1/annurev-food-052720-100326.html?itemId=/content/journals/10.1146/annurev-food-052720-100326&mimeType=html&fmt=ahah

Literature Cited

  1. Abbas S, Wink M 2009. Epigallocatechin gallate (EGCG) from green tea (Camellia sinensis) increases lifespan and stress resistance in Caenorhabditis elegans. . Planta Med. 75:216–21
    [Google Scholar]
  2. Abbas S, Wink M 2010. Epigallocatechin gallate inhibits beta-amyloid oligomerization in Caenorhabditis elegans and affects the daf-2/insulin-like signaling pathway. Phytomedicine 17:902–9
    [Google Scholar]
  3. Abbas S, Wink M 2014. Green tea extract induces the resistance of Caenorhabditis elegans against oxidative stress. Antioxidants 3:129–43
    [Google Scholar]
  4. Al-Ani I, Zimmermann S, Reichling J, Wink M 2015. Pharmacological synergism of bee venom and melittin with antibiotics and plant secondary metabolites against multi-drug resistant microbial pathogens. Phytomedicine 22:245–55
    [Google Scholar]
  5. Alberts B, Johnson A, Lewis J, Raff M, Roberts K, Walter P. 2015. Molecular Biology of the Cell New York: Garland Sci., 6th ed..
    [Google Scholar]
  6. Aleinein R, Hamoud R, Schäfer H, Wink M. 2013. Molecular cloning and expression of ranalexin, a bioactive antimicrobial peptide from Rana catesbeiana, in Escherichia coli and assessment of its biological activities. Appl. Microbiol. Biotechnol. 97:3535–43
    [Google Scholar]
  7. Barardo D, Thornton D, Thoppil H, Walsh M, Sharifi S et al. 2017. The DrugAge database of aging-related drugs. Aging Cell 16:594–97
    [Google Scholar]
  8. Blackwell TK, Steinbaugh MJ, Hourihan JM, Ewald CY, Isik M. 2015. SKN-1/Nrf, stress responses, and aging in Caenorhabditis elegans. Free Radic. . Biol. Med. 88:290–301
    [Google Scholar]
  9. Boasquívis PF, Silva GMM, Paiva FA, Cavalcanti RM, Nunez CV, de Paula Oliveira R. 2018. Guarana (Paullinia cupana) extract protects Caenorhabditis elegans models for Alzheimer disease and Huntington disease through activation of antioxidant and protein degradation pathways. Oxid. Med. Cell. Longev. 2018:9241308
    [Google Scholar]
  10. Brignull HR, Moore FE, Tang SJ, Morimoto RI. 2006. Polyglutamine proteins at the pathogenic threshold display neuron-specific aggregation in a pan-neuronal Caenorhabditis elegans model. J. Neurosci. 26:7597–606
    [Google Scholar]
  11. Chanphai P, Tajmir-Riahi H. 2019. Structural dynamics of DNA binding to tea catechins. Int. J. Biol. Macromol. 125:238–43
    [Google Scholar]
  12. Chen W, Müller D, Richling E, Wink M 2013. Anthocyanin-rich purple wheat prolongs the life span of Caenorhabditis elegans probably by activating the DAF-16/FOXO transcription factor. J Agric. Food Chem. 61:3047–53
    [Google Scholar]
  13. Choi SY, Hwang JH, Ko HC, Park JG, Kim SJ 2007. Nobiletin from citrus fruit peel inhibits the DNA-binding activity of NF-κB and ROS production in LPS-activated RAW 264.7 cells. J. Ethnopharmacol. 113:149–55
    [Google Scholar]
  14. Contreras G, Shirdel I, Braun MS, Wink M. 2020. Defensins: transcriptional regulation and function beyond antimicrobial activity. Dev. Comp. Immunol. 104:103556
    [Google Scholar]
  15. de Freitas Bonomo L, Silva DN, Boasquivis PF, Paiva FA, da Costa Guerra JF et al. 2014. Açaí (Euterpe oleracea Mart.) modulates oxidative stress resistance in Caenorhabditis elegans by direct and indirect mechanisms. PLOS ONE 9:e89933
    [Google Scholar]
  16. Devore EE, Kang JH, Breteler MM, Grodstein F. 2012. Dietary intakes of berries and flavonoids in relation to cognitive decline. Ann. Neurol. 72:135–43
    [Google Scholar]
  17. Domhan C, Uhl P, Kleist C, Zimmermann S, Umstätter F et al. 2019. Replacement of l-amino acids by d-amino acids in the antimicrobial peptide ranalexin and its consequences for antimicrobial activity and biodistribution. Molecules 24:162987
    [Google Scholar]
  18. Domhan C, Uhl P, Zimmermann S, Lindner T, Mier W, Wink M 2018. A novel tool against multiresistant bacterial pathogens: lipopeptide modification of the natural antimicrobial peptide ranalexin for enhanced antimicrobial activity and improved pharmacokinetics. Int. J. Antimicrob. Agents 52:52–62
    [Google Scholar]
  19. Duangjan C, Rangsinth P, Gu X, Wink M, Tencomnao T. 2019a. Lifespan extending and oxidative stress resistance properties of a leaf extracts from Anacardium occidentale L. in Caenorhabditis elegans. Oxid. Med. Cell. Longev. 2019:9012396
    [Google Scholar]
  20. Duangjan C, Rangsinth P, Gu X, Zhang S, Wink M, Tencomnao T. 2019b. Glochidion zeylanicum leaf extracts exhibit lifespan extending and oxidative stress resistance properties in Caenorhabditis elegans via DAF-16/FoxO and SKN-1/Nrf-2 signaling pathways. Phytomedicine 64:153061
    [Google Scholar]
  21. Dziggel C, Schäfer H, Wink M. 2017. Tools of pathway reconstruction and production of economically relevant plant secondary metabolites in recombinant microorganisms. Biotechnol. J. 12:11600145
    [Google Scholar]
  22. Eid SY, El-Readi MZ, Wink M. 2012. Carotenoids reverse multidrug resistance by interfering with ABC-transporters in cancer cells. Phytomedicine 19:977–87
    [Google Scholar]
  23. Fadel O, El Kirat K, Morandat S 2011. The natural antioxidant rosmarinic acid spontaneously penetrates membranes to inhibit lipid peroxidation in situ. Biochim. Biophys. Acta 1808:2973–80
    [Google Scholar]
  24. Fan X, Reichling J, Wink M 2013. Antibacterial activity of the recombinant antimicrobial peptide IB-AMP4 from Impatiens balsamina and its synergy with other antimicrobial agents against drug resistant bacteria. Pharmazie 68:628–30
    [Google Scholar]
  25. Fraga CG, Galleano M, Verstraeten SV, Oteiza PI. 2010. Basic biochemical mechanisms behind the health benefits of polyphenols. Mol. Aspects Med. 31:435–45
    [Google Scholar]
  26. Franceschi C, Garagnani P, Morsiani C, Conte M, Santoro A et al. 2018. The continuum of aging and age-related diseases: common mechanisms but different rates. Front. Med. 5:61
    [Google Scholar]
  27. Frenkel N, Makky I, Resmala Sudji I, Wink M, Tanaka M 2014. Mechanistic investigation of interactions between the steroidal saponin digitonin and cell membrane models. J. Phys. Chem. B 118:14632–39
    [Google Scholar]
  28. Giunti S, Andersen N, Rayes D, De Rosa MJ. 2021. Drug discovery: insights from the invertebrate Caenorhabditis elegans. Pharmacol. Res. Perspect. 9:e00721
    [Google Scholar]
  29. Guerrero-Rubio MA, Hernández-García S, Escribano J, Jiménez-Atiénzar M, Cabanes J et al. 2020. Betalain health-promoting effects after ingestion in Caenorhabditis elegans are mediated by DAF-16/FOXO and SKN-1/Nrf2 transcription factors. Food Chem. 330:127228
    [Google Scholar]
  30. Hamoud R, Reichling J, Wink M 2015a. Synergistic antibacterial activity of the alkaloid sanguinarine with EDTA and the antibiotic streptomycin against multidrug resistant bacteria. J. Pharm. Pharmacol. 67:264–73
    [Google Scholar]
  31. Hamoud R, Reichling J, Wink M 2015b. Synergistic interaction of combinations of sanguinarine and EDTA with vancomycin against multidrug resistant bacteria. Drug Metab. Lett. 8:119–28
    [Google Scholar]
  32. Hamoud R, Zimmermann S, Sporer F, Reichling J, Wink M 2014. Synergistic interactions in two-drug and three-drug combinations (thymol, EDTA and vancomycin) against multidrug resistant bacteria including E. coli. Phytomedicine 21:443–47
    [Google Scholar]
  33. Harborne JB. 1993. Introduction to Ecological Biochemistry London: Academic. , 4th ed..
    [Google Scholar]
  34. Harborne JB, Baxter H. 1993. Phytochemical Dictionary. A Handbook of Bioactive Compounds from Plants London: Taylor Francis
    [Google Scholar]
  35. Hartmann T. 2004. Plant-derived secondary metabolites as defensive chemicals in herbivorous insects: a case study in chemical ecology. Planta 219:1–4
    [Google Scholar]
  36. Hartmann T. 2007. From waste products to ecochemicals: fifty years research of plant secondary metabolism. Phytochemistry 68:2831–46
    [Google Scholar]
  37. Hebestreit P, Melzig MF. 2003. Cytotoxic activity of the seeds from Agrostemma githago var. githago. Planta Med. 69:921–25
    [Google Scholar]
  38. Heiner F, Feistel B, Wink M. 2018. Sideritis scardica extracts inhibit aggregation and toxicity of amyloid-β in Caenorhabditis elegans used as a model for Alzheimer's disease. PeerJ 6:e4683
    [Google Scholar]
  39. Herbel V, Sieber-Frank J, Wink M. 2017. The antimicrobial peptide snakin-2 is upregulated in defence response of tomatoes (Solanum lycopersicum) as part of the JA-dependent signaling pathway. J. Plant Physiol. 208:1–6
    [Google Scholar]
  40. Herbel V, Wink M. 2016. Mode of action and membrane specificity of the antimicrobial peptide snakin-2. PeerJ 4:e1987
    [Google Scholar]
  41. Herrmann F, Hamoud R, Sporer F, Tahrani A, Wink M 2011. Carlina oxide: a natural polyacetylene from Carlina acaulis (Asteraceae) with potent antitrypanosomal and antimicrobial properties. Planta Med. 77:1905–11
    [Google Scholar]
  42. Herrmann F, Wink M 2011. Synergistic interactions of saponins and monoterpenes in HeLa and Cos7 cells and in erythrocytes. Phytomedicine 18:1191–96
    [Google Scholar]
  43. Hertweck M, Göbel C, Baumeister R. 2004. C. elegans SGK-1 is the critical component in the Akt/PKB kinase complex to control stress response and life span. Dev. Cell 6:577–88
    [Google Scholar]
  44. Kampkötter A, Nkwonkam CG, Zurawski RF, Timpel C, Chovolou Y et al. 2007. Effects of the flavonoids kaempferol and fisetin on thermotolerance, oxidative stress and FoxO transcription factor DAF-16 in the model organism Caenorhabditis elegans. Arch. Toxicol. 81:849–58
    [Google Scholar]
  45. Kenyon C. 2011. The first long-lived mutants: discovery of the insulin/IGF-1 pathway for ageing. Philos. Trans. R. Soc. B 366:9–16
    [Google Scholar]
  46. Kim W, Underwood RS, Greenwald I, Shaye DD 2018. OrthoList 2: a new comparative genomic analysis of human and Caenorhabditis elegans genes. Genetics 210:445–61
    [Google Scholar]
  47. Koch K, Weldle N, Baier S, Büchter C, Wätjen W. 2020. Hibiscus sabdariffa L. extract prolongs lifespan and protects against amyloid-β toxicity in Caenorhabditis elegans: involvement of the FoxO and Nrf2 orthologues DAF-16 and SKN-1. Eur. J. Nutr. 59:137–50
    [Google Scholar]
  48. Kotecha R, Takami A, Espinoza JL 2016. Dietary phytochemicals and cancer chemoprevention: a review of the clinical evidence. Oncotarget 7:52517–29
    [Google Scholar]
  49. Krauss GJ, Nies DH. 2014. Ecological Biochemistry: Environmental and Interspecific Interactions. Weinheim, Ger: Wiley-VCH
    [Google Scholar]
  50. Krstin S, Sobeh M, Braun M, Wink M. 2018. Tulbaghia violacea and Allium ursinum extracts exhibit anti-parasitic and antimicrobial properties. Molecules 23:2313
    [Google Scholar]
  51. Labuschagne CF, Brenkman AB. 2013. Current methods in quantifying ROS and oxidative damage in Caenorhabditis elegans and other model organism of aging. Ageing Res. Rev. 12:918–30
    [Google Scholar]
  52. Landis JN, Murphy CT. 2010. Integration of diverse inputs in the regulation of C. elegans DAF-16/FOXO. Dev. Dyn. 239:1405–12
    [Google Scholar]
  53. Lee JM, Johnson JA. 2004. An important role of Nrf2-ARE pathway in the cellular defense mechanism. BMB Rep. 37:139–43
    [Google Scholar]
  54. Lee SS, Kennedy S, Tolonen AC, Ruvkun G. 2003. DAF-16 target genes that control C. elegans life-span and metabolism. Science 300:644–47
    [Google Scholar]
  55. Leonov A, Arlia-Ciommo A, Piano A, Svistkova V, Lutchman V et al. 2015. Longevity extension by phytochemicals. Molecules 20:6544–72
    [Google Scholar]
  56. Leopoldini M, Russo N, Toscano M. 2011. The molecular basis of working mechanism of natural polyphenolic antioxidants. Food Chem 125:288–306
    [Google Scholar]
  57. Li H, Roxo M, Cheng X, Zhang S, Cheng H, Wink M. 2019.. Pro-oxidant and lifespan extension effects of caffeine and related methylxanthines in Caenorhabditis elegans. Food Chem. X 1:100005
    [Google Scholar]
  58. Lima ME, Colpo AC, Salgueiro WG, Sardinha GE, Ávila DS, Folmer V. 2014. Ilex paraguariensis extract increases lifespan and protects against the toxic effects caused by paraquat in Caenorhabditis elegans. Int. J. Environ. Res. Public Health 11:10091–104
    [Google Scholar]
  59. Link CD. 2006. C. elegans models of age-associated neurodegenerative diseases: lessons from transgenic worm models of Alzheimer's disease. Exp. Gerontol. 41:1007–13
    [Google Scholar]
  60. Luo S, Jiang X, Jia L, Tan C, Li M et al. 2019. In vivo and in vitro antioxidant activities of methanol extracts from olive leaves on Caenorhabditis elegans. Molecules 24:4704
    [Google Scholar]
  61. Maeshima M. 2001. Tonoplast transporters: organization and function. Annu. Rev. Plant Physiol. Plant. Mol. Biol. 52:469–97
    [Google Scholar]
  62. Markaki M, Tavernarakis N. 2010. Modeling human diseases in Caenorhabditis elegans. Biotechnol. J. 5:1261–76
    [Google Scholar]
  63. Morley JF, Brignull HR, Weyers JJ, Morimoto RI. 2002. The threshold for polyglutamine-expansion protein aggregation and cellular toxicity is dynamic and influenced by aging in Caenorhabditis elegans. PNAS 99:10417–22
    [Google Scholar]
  64. Mulyaningsih S, Sporer F, Zimmermann S, Reichling J, Wink M 2010. Synergistic properties of the terpenoids aromadendrene and 1,8-cineole from the essential oil of Eucalyptus globulus against antibiotic-susceptible and antibiotic-resistant pathogens. Phytomedicine 17:1061–66
    [Google Scholar]
  65. Murphy CT, McCarroll SA, Bargmann CI, Fraser A, Kamath RS et al. 2003. Genes that act downstream of DAF-16 to influence the lifespan of Caenorhabditis elegans. Nature 424:277–83
    [Google Scholar]
  66. Mursu J, Virtanen JK, Tuomainen T-P, Nurmi T, Voutilainen S. 2014. Intake of fruit, berries, and vegetables and risk of type 2 diabetes in Finnish men: the Kuopio Ischaemic Heart Disease Risk Factor Study. Amer. J. Clin. Nutr. 99:328–33
    [Google Scholar]
  67. Nishioka Y, Nishikawa S, Shibata T 2020. A hot water extract of Sideritis scardica prolongs life span and enhances heat shock resistance in Caenorhabditis elegans. Nat. Prod. Comm. https://doi.org/10.1177/1934578X211020970
    [Crossref] [Google Scholar]
  68. N'Soukpoe-Kossi C, Bourassa P, Mandeville J, Bekale L, Tajmir-Riahi H. 2015. Structural modeling for DNA binding to antioxidants resveratrol, genistein and curcumin. J. Photochem. Photobiol. B 151:69–75
    [Google Scholar]
  69. Oteiza PI, Erlejman AG, Verstraeten SV, Keen CL, Fraga CG. 2005. Flavonoid-membrane interactions: a protective role of flavonoids at the membrane surface?. Clin. Dev. Immunol. 12:19–25
    [Google Scholar]
  70. Ozdal T, Capanoglu E, Altay F 2013. A review on protein–phenolic interactions and associated changes. Food Res. Int. 51:954–70
    [Google Scholar]
  71. Peixoto H, Roxo M, Krstin S, Röhrig T, Richling E, Wink M 2016a. An anthocyanin-rich extract of acai (Euterpe precatoria Mart.) increases stress resistance and retards aging-related markers in Caenorhabditis elegans. J. Agric. Food Chem. 64:1283–90
    [Google Scholar]
  72. Peixoto H, Roxo M, Krstin S, Wang X, Wink M 2016b. Anthocyanin-rich extract of acai (Euterpe precatoria Mart.) mediates neuroprotective activities in Caenorhabditis elegans. J. Funct. Foods 26:385–93
    [Google Scholar]
  73. Peixoto H, Roxo M, Röhrig T, Richling E, Wang X, Wink M. 2017. Anti-aging and antioxidant potential of Paullinia cupana var. sorbilis: findings in Caenorhabditis elegans indicate a new utilization for roasted seeds of guarana. Medicines 4:361
    [Google Scholar]
  74. Peixoto H, Roxo M, Silva E, Valente K, Braun M et al. 2019. Bark extract of the Amazonian tree Endopleura uchi (Humiriaceae) extends lifespan and enhances stress resistance in Caenorhabditis elegans. Molecules 24:5915
    [Google Scholar]
  75. Perron NR, Brumaghim JL. 2009. A review of the antioxidant mechanisms of polyphenol compounds related to iron binding. Cell Biochem. Biophys. 53:75–100
    [Google Scholar]
  76. Prasanth MI, Brimson JM, Chuchawankul S, Sukprasansap M, Tencomnao T. 2019. Antiaging, stress resistance, and neuroprotective efficacies of Cleistocalyx nervosum var. paniala fruit extracts using Caenorhabditis elegans model. Oxid. Med. Cell. Longev. 2019:7024785
    [Google Scholar]
  77. Qi Z, Ji H, Le M, Li H, Wieland A et al. 2021. Sulforaphane promotes C. elegans longevity and healthspan by DAF-16/DAF-2 insulin/IGF-1 signaling. Aging 13:1649–70
    [Google Scholar]
  78. Rangsinth P, Prasansuklab A, Duangjan C, Gu X, Meemon K et al. 2019. Leaf extract of Caesalpinia mimosoides enhances oxidative stress resistance and prolongs lifespan in Caenorhabditis elegans. BMC Complement. Altern. Med. 19:164
    [Google Scholar]
  79. Reddy KV, Yedery RD, Aranha C. 2004. Antimicrobial peptides: premises and promises. Int. J. Antimicrob. Agents 24:536–47
    [Google Scholar]
  80. Regitz C, Fitzenberger E, Mahn FL, Dußling LM, Wenzel U. 2016. Resveratrol reduces amyloid-beta (Aβ 1–42)-induced paralysis through targeting proteostasis in an Alzheimer model of Caenorhabditis elegans. Eur. J. Nutr. 55:741–47
    [Google Scholar]
  81. Rehman R, Hanif MA, Mushtaq Z, Mochona B, Qi X 2016. Biosynthetic factories of essential oils: the aromatic plants. Nat. Prod. Chem. Res. 4:1000227
    [Google Scholar]
  82. Reichling J 2010. Plant-microbe interactions and secondary metabolites with antibacterial, antifungal and antiviral properties. Functions and Biotechnology of Plant Secondary Metabolites, Vol. 39 M Wink 214–347 Chichester, UK: Wiley-Blackwell
    [Google Scholar]
  83. Robida-Stubbs S, Glover-Cutter K, Lamming DW, Mizunuma M, Narasimhan SD et al. 2012. TOR signaling and rapamycin influence longevity by regulating SKN-1/Nrf and DAF-16/FoxO. Cell Metab. 15:713–24
    [Google Scholar]
  84. Roxo M, Peixoto H, Wetterauer P, Lima E, Wink M. 2020. Piquiá shells (Caryocar villosum): a fruit by-product with antioxidant and antiaging properties in Caenorhabditis elegans. Oxid. Med. Cell. Longev. 2020:7590707
    [Google Scholar]
  85. Saier C, Gommlich I, Hiemann V, Baier S, Koch K et al. 2018. Agrimonia procera Wallr. extract increases stress resistance and prolongs life span in Caenorhabditis elegans via transcription factor DAF-16 (FoxO orthologue). Antioxidants 7:12192
    [Google Scholar]
  86. Scalbert A, Manach C, Morand C, Rémésy C, Jiménez L 2005. Dietary polyphenols and the prevention of diseases. Crit. Rev. Food Sci. Nutr. 45:287–306
    [Google Scholar]
  87. Scerbak C, Vayndorf E, Hernandez A, McGill C, Taylor B. 2018. Lowbush cranberry acts through DAF-16/FOXO signaling to promote increased lifespan and axon branching in aging posterior touch receptor neurons. Geroscience 40:151–62
    [Google Scholar]
  88. Seigler DS. 1998. Plant Secondary Metabolism Dordrecht, Neth: Kluwer
    [Google Scholar]
  89. Senchuk MM, Dues D, Van Raamsdonk JM. 2017. Measuring oxidative stress in Caenorhabditis elegans: paraquat and juglone sensitivity assays. Bio-Protocol 7:e2086
    [Google Scholar]
  90. Sies H, Jones DP. 2020. Reactive oxygen species (ROS) as pleiotropic physiological signalling agents. Nat. Rev. Mol. Cell Biol. 21:363–83
    [Google Scholar]
  91. Sirk TW, Brown EF, Friedman M, Sum AK. 2009. Molecular binding of catechins to biomembranes: relationship to biological activity. J. Agric. Food Chem. 57:6720–28
    [Google Scholar]
  92. Sobeh M, ElHawary E, Peixoto H, Labib RM, Handoussa H et al. 2016. Identification of phenolic secondary metabolites from Schotia brachypetala Sond. (Fabaceae) and demonstration of their antioxidant activities in Caenorhabditis elegans. PeerJ 4:e2404
    [Google Scholar]
  93. Sobeh M, Mahmoud MF, Abdelfattah MA, Cheng H, El-Shazly AM, Wink M. 2018. A proanthocyanidin-rich extract from Cassia abbreviata exhibits antioxidant and hepatoprotective activities in vivo. J. Ethnopharm. 213:38–47
    [Google Scholar]
  94. Strange K. 2006. An overview of C. elegans biology. Methods Mol. Biol. 351:1–11
    [Google Scholar]
  95. Sudji IR, Subburaj Y, Frenkel N, García-Sáez AJ, Wink M. 2015. Membrane disintegration caused by the steroid saponin digitonin is related to presence of cholesterol. Molecules 20:20146–60
    [Google Scholar]
  96. Tambara AL, de los Santos Moraes L, Dal Forno AH, Boldori JR, Soares ATG et al. 2018. Purple pitanga fruit (Eugenia uniflora L.) protects against oxidative stress and increase the lifespan in Caenorhabditis elegans via the DAF-16/FOXO pathway. Food Chem. Toxicol. 120:639–50
    [Google Scholar]
  97. Thabit S, Handoussa H, Roxo M, El Sayed NS, de Azevedo BC, Wink M. 2018. Evaluation of antioxidant and neuroprotective activities of Cassia fistula (L.) using the Caenorhabditis elegans model. PeerJ 6:e5159
    [Google Scholar]
  98. Theodoulou FL, Kerr ID. 2015. ABC transporter research: going strong 40 years on. Biochem. Soc. Trans. 43:1033–40
    [Google Scholar]
  99. Tullet JM, Hertweck M, An JH, Baker J, Hwang JY et al. 2008. Direct inhibition of the longevity-promoting factor SKN-1 by insulin-like signaling in C. elegans. Cell 132:1025–38
    [Google Scholar]
  100. Van Wyk BE. 2014. Culinary Herbs & Spices of the World Pretoria, S. Afr.: BRIZA
    [Google Scholar]
  101. Van Wyk BE, Wink M. 2015. Phytomedicines, Herbal Drugs and Poisons London: Kew Publ.
    [Google Scholar]
  102. Van Wyk BE, Wink M. 2017. Medicinal Plants of the World Wallingford, UK: CABI. , 2nd ed..
    [Google Scholar]
  103. Wagner H, Ulrich-Merzenich G. 2009. Synergy research: approaching a new generation of phytopharmaceuticals. Phytomedicine 16:97–110
    [Google Scholar]
  104. Wang E, Wink M 2016. Chlorophyll enhances oxidative stress tolerance in Caenorhabditis elegans and extends its lifespan. PeerJ 4:e1879
    [Google Scholar]
  105. Wang H, Liu J, Li T, Liu RH 2018. Blueberry extract promotes longevity and stress tolerance via DAF-16 in Caenorhabditis elegans. Food Funct 9:5273–82
    [Google Scholar]
  106. Wang S, Melnyk JP, Tsao R, Marcone MF. 2011. How natural dietary antioxidants in fruits, vegetables and legumes promote vascular health. Food Res. Int. 44:14–22
    [Google Scholar]
  107. Wink M. 1988. Plant breeding: importance of plant secondary metabolites for protection against pathogens and herbivores. Theor. Appl. Genet. 75:225–33
    [Google Scholar]
  108. Wink M. 1997. Compartmentation of secondary metabolites and xenobiotics in plant vacuoles. Adv. Bot. Res. 25:141–69
    [Google Scholar]
  109. Wink M. 2000. Interference of alkaloids with neuroreceptors and ion channels. Stud. Nat. Prod. Chem. 21:3–122
    [Google Scholar]
  110. Wink M. 2003. Evolution of secondary metabolites from an ecological and molecular phylogenetic perspective. Phytochemistry 64:3–19
    [Google Scholar]
  111. Wink M. 2007. Molecular modes of action of cytotoxic alkaloids: from DNA intercalation, spindle poisoning, topoisomerase inhibition to apoptosis and multiple drug resistance. Alkaloids 64:1–47
    [Google Scholar]
  112. Wink M. 2008a. Evolutionary advantage and molecular modes of action of multi-component mixtures used in phytomedicine. Curr. Drug Metab. 9:996–1009
    [Google Scholar]
  113. Wink M. 2008b. Plant secondary metabolism: diversity, function and its evolution. Nat. Prod. Comm. 3:1205–16
    [Google Scholar]
  114. Wink M. 2010a. Biochemistry of Plant Secondary Metabolism Chichester, UK: Wiley-Blackwell. , 2nd ed..
    [Google Scholar]
  115. Wink M. 2010b. Function of Plant Secondary Metabolites and Their Exploitation in Biotechnology Chichester, UK: Wiley-Blackwell
    [Google Scholar]
  116. Wink M. 2013. Evolution of secondary metabolites in legumes (Fabaceae). South Afr. . J. Bot. 89:164–75
    [Google Scholar]
  117. Wink M. 2015. Modes of action of herbal medicines and plant secondary metabolites. Medicines 2:251–86
    [Google Scholar]
  118. Wink M. 2018. Plant secondary metabolites modulate insect behaviour: steps toward addiction?. Front. Physiol. 9:364
    [Google Scholar]
  119. Wink M. 2019. Quinolizidine and pyrrolizidine alkaloid chemical ecology: a mini-review on their similarities and differences. J. Chem. Ecol. 45:109–15
    [Google Scholar]
  120. Wink M 2020a. Evolution of the angiosperms and co-evolution of secondary metabolites, especially of alkaloids. Co-Evolution of Secondary Metabolites J-M Mérillon, KG Ramawat 1–24 Baskingstoke, UK: Springer Nat.
    [Google Scholar]
  121. Wink M. 2020b. Potential of DNA intercalating alkaloids and other plant secondary metabolites against SARS-CoV-2 causing COVID-19. Diversity 12:5175
    [Google Scholar]
  122. Wink M, Schimmer O 2010. Molecular modes of action of defensive secondary metabolites. Functions and Biotechnology of Plant Secondary Metabolites M Wink 21–161 Chichester, UK: Wiley-Blackwell
    [Google Scholar]
  123. Wink M, Van Wyk BE. 2008. Mind-Altering and Poisonous Plants of the World Portland, OR: Timber Press
    [Google Scholar]
  124. Wu Y, Wu Z, Butko P, Christen Y, Lambert MP et al. 2006. Amyloid-β-induced pathological behaviors are suppressed by Ginkgo biloba extract EGb 761 and ginkgolides in transgenic Caenorhabditis elegans. J. Neurosci. 26:13102–13
    [Google Scholar]
  125. Zamberlan D, Amaral G, Arantes L, Machado M, Mizdal C et al. 2016. Rosmarinus officinalis L. increases Caenorhabditis elegans stress resistance and longevity in a DAF-16, HSF-1 and SKN-1-dependent manner. Braz. J. Med. Biol. Res. 49:9e5235
    [Google Scholar]
  126. Zenk MH, Jünger M. 2007. Evolution and current status of the phytochemistry of nitrogenous compounds. Phytochemistry 65:2757–72
    [Google Scholar]
  127. Zhang S, Duangjan C, Tencomnao T, Liu J, Wink M, Lin J. 2020. Neuroprotective effects of oolong tea extracts against glutamate-induced toxicity in cultured neuronal cells and Aβ-induced toxicity in Caenorhabditis elegans. . Food Func. 11:8179–92
    [Google Scholar]
/content/journals/10.1146/annurev-food-052720-100326
Loading
/content/journals/10.1146/annurev-food-052720-100326
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error