Skip to main content
Log in

Anthocyanins in corn: a wealth of genes for human health

  • Review
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Different epidemiological and preclinical studies have demonstrated that regular consumption of anthocyanin-rich foods is associated to a reduced risk of chronic diseases, such as cardiovascular diseases, cancer and obesity. However, assigning a health property to anthocyanins or other classes of flavonoids may be limited by the influence of other metabolites of plant-based food consumed in the diet, acting as possible confounding factors. The development of model foods essentially isogenic and nutritionally identical except that in the type and quantity of plant bioactives to be studied represents an important tool in nutritional studies. The extensive knowledge of the regulation of flavonoid pathway in maize can be exploited to obtain ‘near-isogenic’ model foods, which differ only in the content of specific classes of flavonoids. Being obtainable by breeding strategies, maize model foods can provide functional foods that can be used for both animal feeding studies and human intervention trials for assessing the role of flavonoids or other bioactives in preventing chronic diseases. This review will be focused on recent advances regarding the anthocyanin biosynthesis in maize, the role of anthocyanins from corn in preventing chronic diseases and finally on the breeding activities to produce maize functional foods with increased anthocyanin content.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

r1 :

red color1

b1 :

booster1

c1 :

colored aleurone1 or colorless1

pl1 :

purple plant1

p1 :

pericarp color1

pr1 :

purple aleurone1

bHLH:

Basic helix-loop-helix

CHS:

Chalcone synthase

CHI:

Chalcone isomerase

F3H:

Flavanone 3-hydroxylase

F3′H:

Flavanone 3′-hydroxylase

DFR:

Dihydroflavonol reductase

FLS:

Flavonol synthase

ANS:

Anthocyanidin synthase

DHK:

Dihydrokaempferol

DHQ:

Dihydroquercetin

References

  • Andersen ØM, Fossen T (1995) Anthocyanins with an unusual acylation pattern from stem of Allium victorialis. Phytochemistry 40:1809–1812

    Article  CAS  Google Scholar 

  • Berman J, Zhu C, Perez-Massot E, Arjo´ G, Zorrilla-Lopez U, Masip G, Banakar R, Sanahuja G, Farre´ G, Miralpeix B, Bai C, Vamvaka E, Sabalza M, Twyman RM, Bassie´ L, Capell T, Christou P (2013) Can the world afford to ignore biotechnology solutions that address food insecurity? Plant Mol Biol 83:5–19

    Article  PubMed  CAS  Google Scholar 

  • Brandolini A, Brandolini A (2009) Maize introduction, evolution and diffusion in Italy. Maydica 54:233–242

    Google Scholar 

  • Butelli E, Titta L, Giorgio M, Mock HP, Matros A, Peterek S, Schijlen EGWM, Hall RD, Bovy AG, Luo J, Martin C (2008) Enrichment of tomato fruit with health-promoting anthocyanins by expression of select transcription factors. Nat Biotechnol 26:1301–1308

    Article  PubMed  CAS  Google Scholar 

  • Carey CC, Strahle JT, Selinger DA, Chandler VL (2004) Mutations in the pale aleurone color1 regulatory gene of the Zea mays anthocyanin pathway have distinct phenotypes relative to the functionally similar TRANSPARENT TESTA GLABRA1 gene in Arabidopsis thaliana. Plant Cell 16:450–464

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Cassidy A, Mukamal KJ, Liu L, Franz M, Eliassen AH, Rimm EB (2013) High anthocyanin intake is associated with a reduced risk of myocardial infarction in young and middle-aged women. Circulation 127:188–196

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Cevallos-Casals BA, Cisneros-Zevallos L (2003) Stoichiometric and kinetic studies of phenolic antioxidants from Andean purple corn and red-fleshed sweet potato. J Agr Food Chem 51:3313–3319

    Article  CAS  Google Scholar 

  • Chandler VL, Radicella JP, Robbins Chen JC, Turks D (1989) Two regulatory genes of the maize anthocyanin pathway are homologous: isolation of B utilizing R genomic sequences. Plant Cell 1:1175–1183

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Chapman JS, Steele FM, Eggett DL, Johnston NP, Dunn ML (2010) Stability of native folate and added folic acid in micronutrient-fortified corn masa and tortillas. Cereal Chem 87:434–438

    Article  CAS  Google Scholar 

  • Cocciolone SM, Cone KC (1993) Pl-Bh, an anthocyanin regulatory gene of maize that leads to variegated pigmentation. Genetics 135:575–588

    PubMed  CAS  PubMed Central  Google Scholar 

  • Dooner HK, Robbins TP, Jorgensen RA (1991) Genetic and developmental control of anthocyanin biosynthesis. Annu Rev Genet 25:173–199

    Article  PubMed  CAS  Google Scholar 

  • Escribano-Bailόn MT, Santos-Buelga C, Rivas-Gonzalo JC (2004) Anthocyanins in cereals. J Chromatogr A 1054:129–141

    Article  Google Scholar 

  • Ferreyra ML, Rius S, Emiliani J, Pourcel L, Feller A, Morohashi K et al (2010) Cloning and characterization of a UV-B-inducible maize flavonol synthase. Plant J 62:77–91

    Article  CAS  Google Scholar 

  • Food and Agriculture Organization of the United Nations (2009) Crops Production. http://faostat.fao.org/site/567/DesktopDefault.aspx?PageID=567. Accessed 20 April 2011

  • Fossen T, Slimestad R, Andersen OM (2001) Anthocyanins from maize (Zea mays) and reed canary grass (Phalaris arundinacea). J Agric Food Chem 49:2318–2321

    Article  PubMed  CAS  Google Scholar 

  • Fossen T, Slimestad R, Øvstedal DO, Andersen ØM (2002) Anthocyanins of grasses. Biochem Syst Ecol 30:855–864

    Article  CAS  Google Scholar 

  • Fukamachi K, Imada T, Ohshima Y, Xu J, Tsuda H (2008) Purple corn color suppresses Ras protein level and inhibits 7,12-dimethylbenz[a]anthracene-induced mammary carcinogenesis in the rat. Cancer Sci 99:1841–1846

    Article  PubMed  CAS  Google Scholar 

  • Giusti MM, Wrolstad RE (2003) Acylated anthocyanins from edible sources and their applications in food systems. Biochem Eng J 14:217–225

    Article  CAS  Google Scholar 

  • Goff SA, Cone KC, Chandler VL (1992) Functional analysis of the transcriptional activator encoded by the maize B gene: evidence for a direct functional interaction between two classes of regulatory proteins. Genes Dev 6:864–875

    Article  PubMed  CAS  Google Scholar 

  • Grotewold E, Drummond BJ, Bowen B, Peterson T (1994) The myb-homologous P gene controls phlobaphene pigmentation in maize floral organs by directly activating a flavonoid biosynthetic gene subset. Cell 76:543–553

    Article  PubMed  CAS  Google Scholar 

  • Hagiwara A, Miyashita K, Nakanishi T, Sano M, Tamano S, Kadota T, Koda T, Nakamura M, Imaida K, Ito N, Shirai T (2001) Pronounced inhibition by a natural anthocyanin, purple corn color, of 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP)-associated colorectal carcinogenesis in male F344 rats pretreated with 1,2-dimethylhydrazine. Cancer Lett 171:17–25

    Article  PubMed  CAS  Google Scholar 

  • Hollick JB, Patterson GI, Coe EH Jr, Cone KC, Chandler VL (1995) Allelic interactions heritably alter the activity of a metastable maize pl1 allele. Genetics 141:709–719

    PubMed  CAS  PubMed Central  Google Scholar 

  • Humble CG, Malarcher AM, Tyroler HA (1993) Dietary fiber and coronary heart disease in middle-aged hypercholesterolemic men. Am J Prev Med 9:197–202

    PubMed  CAS  Google Scholar 

  • Jennings A, Welch AA, Spector T, Macgregor A, Cassidy A (2014) Intakes of anthocyanins and flavones are associated with biomarkers of insulin resistance and inflammation in women. J Nutr 144:202–208

    Article  PubMed  CAS  Google Scholar 

  • Juvik JA, Yousef GG, Han TH, Tadmor Y, Azanza F, Tracy WF, Barzur A, Rocheford TR (2003) QTL influencing kernel chemical composition and seedling stand establishment in sweet corn with the shrunken2 and sugary enhancer1 endosperm mutations. J Am Soc Hort Sci 128:864–875

    CAS  Google Scholar 

  • Kang MK, Li J, Kim JL, Gong JH, Kwak SN, Park JH, Lee JY, Lim SS, Kang YH (2012) Purple corn anthocyanins inhibit diabetes-associated glomerular monocyte activation and macrophage infiltration. Am J Physiol Renal Physiol 303:F1060–F1069

    Article  PubMed  CAS  Google Scholar 

  • Kang MK, Lim SS, Lee JY, Yeo KM, Kang YH (2013) Anthocyanin-rich purple corn extract inhibit diabetes-associated glomerular angiogenesis. PLoS One 8:e79823

    Article  PubMed  PubMed Central  Google Scholar 

  • Karababa E (2006) Physical properties of popcorn kernels. J Food Eng 72:100–107

    Article  Google Scholar 

  • Kong Q, Pattanaik S, Feller A, Werkman JR, Chai C, Wang Y et al (2012) Regulatory switch enforced by basic helix-loop-helix and ACT-domain mediated dimerizations of the maize transcription factor R. Proc Natl Acad Sci USA 109:E2091–E2097

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Lago C, Landoni M, Cassani E, Doria E, Nielsen E, Pilu R (2013) Study and characterization of a novel functional food: purple popcorn. Mol Breeding 31:575–585

    Article  CAS  Google Scholar 

  • Lago C, Cassani E, Zanzi C, Landoni M, Trovato R, Pilu R (2014) Development and study of a maize cultivar rich in anthocyanins: coloured polenta, a new functional food. Plant Breeding. doi:10.1111/pbr.12153

    Google Scholar 

  • Li J, Kang MK, Kim JK, Kim JL, Kang SW, Lim SS et al (2012a) Purple corn anthocyanins retard diabetes-associated glomerulosclerosis in mesangial cells and db/db mice. Eur J Nutr 51:961–973

    Article  PubMed  Google Scholar 

  • Li J, Lim SS, Lee JY, Kim JK, Kang SW, Kim JL et al (2012b) Purple corn anthocyanins dampened high-glucose-induced mesangial fibrosis and inflammation: possible renoprotective role in diabetic nephropathy. J Nutr Biochem 23:320–331

    Article  PubMed  CAS  Google Scholar 

  • Liu S, Stampfer MJ, Hu FB, Giovannucci E, Rimm E, Manson JE et al (1999) Whole-grain consumption and risk of coronary heart disease: results from the Nurses’ Health Study. Am J Clin Nutr 70:412–419

    PubMed  CAS  Google Scholar 

  • Long N, Suzuki S, Sato S, Naiki-Ito A, Sakatani K, Shirai T, Takahashi S (2013) Purple corn color inhibition of prostate carcinogenesis by targeting cell growth pathways. Cancer Sci 104:298–303

    Article  PubMed  CAS  Google Scholar 

  • Martin C, Butelli E, Petroni K, Tonelli C (2011) How can research on plants contribute to promoting human health? Plant Cell 23:1685–1699

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Martin C, Zhang Y, Tonelli C, Petroni K (2013) Plants, diet, and health. Annu Rev Plant Biol 64:19–46

    Article  PubMed  CAS  Google Scholar 

  • McCarty DR, Carson CB, Stinard PS, Robertson DS (1989) Molecular analysis of viviparous-1: an abscisic acid-insensitive mutant of maize. Plant Cell 1:523–532

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • McCullough ML, Feskanich D, Stampfer MJ, Giovannucci EL, Rimm EB, Hu FB et al (2002) Diet quality and major chronic disease risk in men and women: moving toward improved dietary guidance. Am J Clin Nutr 76:1261–1271

    PubMed  CAS  Google Scholar 

  • Meyer KA, Kushi LH, Jacobs DR Jr, Slavin J, Sellers TA, Folsom AR (2000) Carbohydrates, dietary fiber, and incident type 2 diabetes in older women. Am J Clin Nutr 71:921–930

    PubMed  CAS  Google Scholar 

  • Muller M, Kersten S (2003) Nutrigenomics: goals and strategies. Nat Rev Genet 4:315–322

    Article  PubMed  Google Scholar 

  • Nakayama M, Koshioka M, Shibata M, Hiradate S, Sugie H, Yamaguchi M (1997) Identification of cyaniding 3-O-(3″,6″-O-dimalonyl-β-glucopyranoside) as a flower pigment of chrysanthemum (Dendranthema grandiflorum). Biosci Biotechnol Biochem 61:1607–1608

    Article  CAS  Google Scholar 

  • Nakayama T, Suzuki H, Nishino T (2003) Anthocyanin acyltransferases: specificities, mechanism, phylogenetics, and applications. J Mol Catal B Enzym 23:117–132

    Article  CAS  Google Scholar 

  • Panzeri D, Cesari V, Toschi I, Pilu R (2011) Seed calorific value in different maize genotypes. Energy Sources Part A Recover Utilization Environ Effects 33:1700–1705

    Article  Google Scholar 

  • Petroni K, Tonelli C (2011) Recent advances on the regulation of anthocyanin synthesis in reproductive organs. Plant Sci 181:219–229

    Article  PubMed  CAS  Google Scholar 

  • Petroni K, Cominelli E, Consonni G, Gusmaroli G, Gavazzi G, Tonelli C (2000) The developmental expression of the maize regulatory gene Hopi determines germination-dependent anthocyanin accumulation. Genetics 155:323–336

    PubMed  CAS  PubMed Central  Google Scholar 

  • Pilu R (2011) Paramutation: just a curiosity or fine tuning of gene expression in the next generation? Curr Genomics 12:298–306

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Pilu R, Piazza P, Petroni K, Ronchi A, Martin C, Tonelli C (2003) pl-bol3, a complex allele of the anthocyanin regulatory pl1 locus that arose in a naturally occurring maize population. Plant J 36:510–521

    Article  PubMed  CAS  Google Scholar 

  • Pilu R, Cassani E, Sirizzotti A, Petroni K, Tonelli C (2011) Effect of flavonoid pigments on the accumulation of fumonisin B1 in the maize kernel. J Appl Genet 52:145–152

    Article  PubMed  CAS  Google Scholar 

  • Procissi A, Dolfini S, Ronchi A, Tonelli C (1997) Light-dependent spatial and temporal expression of pigment regulatory genes in developing maize seeds. Plant Cell 9:1547–1557

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Renaud S, de Lorgeril M (1992) Wine, alcohol, platelets, and the French paradox for coronary heart disease. Lancet 339:1523–1526

    Article  PubMed  CAS  Google Scholar 

  • Rodriguez-Amaya DB, Kimura M, Godoy HT, Amaya-Farfan J (2008) Updated Brazilian database on food carotenoids: factors affecting carotenoid composition. J Food Compos Anal 21:445–463

    Article  CAS  Google Scholar 

  • Sainz MB, Grotewold E, Chandler VL (1997) Evidence for direct activation of an anthocyanin promoter by the maize C1 protein and comparison of DNA binding by related Myb domain proteins. Plant Cell 9:611–625

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Saito D, Maeshima Y, Nasu T, Yamasaki H, Tanabe K, Sugiyama H, Sonoda H, Sato Y, Makino H (2011) Amelioration of renal alterations in obese type 2 diabetic mice by vasohibin-1, a negative feedback regulator of angiogenesis. Am J Physiol Renal Physiol 300:F873–F886

    Article  PubMed  CAS  Google Scholar 

  • Schwarz M, Hillebrand S, Habben S, Degenhardt A, Winterhalter P (2003) Application of high-speed countercurrent chromatography to the large-scale isolation of anthocyanins. Biochem Eng J 14:179–189

    Article  CAS  Google Scholar 

  • Sebrell WH (1981) History of pellagra. Federation Proc 40:1520–1522

    Google Scholar 

  • Selinger DA, Chandler VL (1999) A mutation in the pale aleurone color1 gene identifies a novel regulator of the maize anthocyanin pathway. Plant Cell 11:5–14

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Sharma M, Cortes-Cruz M, Ahern KR, McMullen M, Brutnell TP, Chopra S (2011) Identification of the Pr1 gene product completes the anthocyanin biosynthesis pathway of maize. Genetics 188:69–79

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Sharma M, Chai C, Morohashi K, Grotewold E, Snook ME, Chopra S (2012) Expression of flavonoid 3′-hydroxylase is controlled by P1, the regulator of 3-deoxyflavonoid biosynthesis in maize. BMC Plant Biol 12:196

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Suzuki H, Nakayama T, Yamaguchi M-A, Nishino T (2004) cDNA cloning and characterization of two Dendranthema x morifolium anthocyanin malonyltransferases with different functional activities. Plant Sci 166:89–96

    Article  CAS  Google Scholar 

  • Tonelli C, Consonni G, Dolfini SF, Dellaporta SL, Viotti A, Gavazzi G (1991) Genetic and molecular analysis of Sn, a light-inducible, tissue specific regulatory gene in maize. Mol Gen Genet 225:401–410

    Article  PubMed  CAS  Google Scholar 

  • Toufektsian MC, de Lorgeril M, Nagy N, Salen P, Donati MB, Giordano L et al (2008) Chronic dietary intake of plant-derived anthocyanins protects the rat heart against ischemia-reperfusion injury. J Nutr 138:747–752

    PubMed  CAS  Google Scholar 

  • Toufektsian MC, Salen P, Laporte F, Tonelli C, de Lorgeril M (2011) Dietary flavonoids increase plasma very long-chain (n-3) fatty acids in rats. J Nutr 141:37–41

    Article  PubMed  CAS  Google Scholar 

  • Tsuda T (2012) Dietary anthocyanin-rich plants: biochemical basis and recent progress in health benefits studies. Mol Nutr Food Res 56:159–170

    Article  PubMed  CAS  Google Scholar 

  • Tsuda T, Horio F, Uchida K, Aoki H, Osawa T (2003) Dietary cyanidin 3-O-β-D-glucoside-rich purple corn color prevents obesity and ameliorates hyperglycemia in mice. J Nutr 133:2125–2130

    PubMed  CAS  Google Scholar 

  • Villalpando S (2004) Tortilla fortification working group meeting. El problema de la biodisponibilidad de hierro en harina de maiz nixtamalizada. National Institute of Public Health, Mexico City

  • Werner MS (1997) Encyclopedia of Mexico: history, society and culture. Fitzroy Dearborn, Chicago

    Google Scholar 

  • Winkel-Shirley B (2002) Biosynthesis of flavonoids and effects of stress. Curr Opin Plant Biol 5:218–223

    Article  PubMed  CAS  Google Scholar 

  • Wu X, Beecher GR, Holden JM, Haytowitz DB, Gebhardt SE, Prior RL (2006) Concentrations of anthocyanins in common foods in the United States and estimation of normal consumption. J Agric Food Chem 54:4069–4075

    Article  PubMed  CAS  Google Scholar 

  • Zent R, Pozzi A (2007) Angiogenesis in diabetic nephropathy. Semin Nephrol 27:161–171

    Article  PubMed  CAS  Google Scholar 

  • Zeppa G, Bertolino M, Rolle L (2012) Quantitative descriptive analysis of Italian polenta produced with different corn cultivars. J Sci Food Agr 92:412–417

    Article  CAS  Google Scholar 

  • Ziegler KE, Ashman RB, White GM, Wysong DS (1984) Popcorn production and marketing. National corn handbook, NCH-5, Purdue University, West Lafayette, Indiana

Download references

Acknowledgments

This work was supported by the EU FP7 ATHENA collaborative project (Grant Agreement 245121) to CT, by Regione Lombardia Fondo per la promozione di Accordi Istituzionali (project BIOGESTECA 15083/RCC) to CT and RP, and by Fondazione Umberto Veronesi Grant 2012 to KP.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Katia Petroni.

Additional information

Special topic: Anthocyanins. Guest editor: Stefan Martens.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Petroni, K., Pilu, R. & Tonelli, C. Anthocyanins in corn: a wealth of genes for human health. Planta 240, 901–911 (2014). https://doi.org/10.1007/s00425-014-2131-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-014-2131-1

Keywords

Navigation