Skip to main content
Log in

MpigE, a gene involved in pigment biosynthesis in Monascus ruber M7

  • Applied genetics and molecular biotechnology
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Monascus pigments (MPs) have been used as food colorants for several centuries in Asian countries. However, MP biosynthesis pathway is still a controversy, and only few related genes have been reported. In this study, the function of MpigE, a gene involved in MP biosynthesis in Monascus ruber M7, was analyzed. The results revealed that the disruption, complementation, and overexpression of MpigE in M. ruber M7 had very little effects on the growth and phenotypes except MPs. The MpigE deletion strain (∆MpigE) just yielded four kinds of yellow MPs and very little red pigments, while the wild-type strain M. ruber M7 produced a MP complex mixture including three (orange, red, and yellow) categories of MP compounds. Two of the four yellow MPs produced by ∆MpigE were the same as those yielded by M. ruber M7. The MpigE complementation strain (∆MpigE::MpigE) recovered the ability to generate orange and red MPs as M. ruber M7. The MP types produced by the MpigE overexpression strain (M7::PtrpC-MpigE) were consistent with those of M. ruber M7, while the color value was about 1.3-fold as that of M. ruber M7 (3,129 U/g red kojic). For the production of citrinin, the disruption of MpigE almost had no influence on the strain, whereas the overexpression of MpigE made citrinin decrease drastically in YES fermentation. This work will make a contribution to the study on the biosynthesis pathway of MPs in M. ruber.

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
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Akihisa T, Tokuda H, Yasukawa K, Ukiya M, Kiyota A, Sakamoto N, Suzuki T, Tanabe N, Nishino H (2005a) Azaphilones, furanoisophthalides, and amino acids from the extracts of Monascus pilosus-fermented rice (red-mold rice) and their chemopreventive effects. J Agric Food Chem 53(3):562–565. doi:10.1021/jf040199p

    Article  CAS  PubMed  Google Scholar 

  • Akihisa T, Tokuda H, Ukiya M, Kiyota A, Yasukawa K, Sakamoto N, Kimura Y, Suzuki T, Takayasu J, Nishino H (2005b) Anti-tumor-initiating effects of monascin, an azaphilonoid pigment from the extract of Monascus pilosus fermented rice (red-mold rice). Chem Biodivers 2(10):1305–1309. doi:10.1002/cbdv.200590101

    Article  CAS  PubMed  Google Scholar 

  • Balakrishnan B, Karki S, Chiu S-H, Kim H-J, Suh J-W, Nam B, Yoon Y-M, Chen C-C, Kwon H-J (2013) Genetic localization and in vivo characterization of a Monascus azaphilone pigment biosynthetic gene cluster. Appl Microbiol Biotechnol 97(14):6337–6345. doi:10.1007/s00253-013-4745-9

    Article  CAS  PubMed  Google Scholar 

  • Chen F, Hu X (2005) Study on red fermented rice with high concentration of monacolin K and low concentration of citrinin. Int J Food Microbiol 103(3):331–337. doi:10.1016/j.ijfoodmicro.2005.03.002

    Article  CAS  PubMed  Google Scholar 

  • Chen W, Xie T, Shao Y, Chen F (2012a) Genomic characteristics comparisons of 12 food-related filamentous fungi in tRNA gene set, codon usage and amino acid composition. Gene 497(1):116–124. doi:10.1016/j.gene.2012.01.016

    Article  CAS  PubMed  Google Scholar 

  • Chen W, Xie T, Shao Y, Chen F (2012b) Phylogenomic relationships between amylolytic enzymes from 85 strains of fungi. PLoS One 7(11):e49679. doi:10.1371/journal.pone.0049679

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Choe D, Lee J, Woo S, Shin CS (2012) Evaluation of the amine derivatives of Monascus pigment with anti-obesity activities. Food Chem 134(1):315–323. doi:10.1016/j.foodchem.2012.02.149

    Article  CAS  Google Scholar 

  • Dufossé L, Galaup P, Yaron A, Arad SM, Blanc P, Chidambara Murthy KN, Ravishankar GA (2005) Microorganisms and microalgae as sources of pigments for food use: a scientific oddity or an industrial reality? Trends Food Sci Technol 16(9):389–406. doi:10.1016/j.tifs.2005.02.006

    Article  Google Scholar 

  • Endo A (1979) Monacolin-K, a new hypocholesterolemic agent produced by a Monascus species. J Antibiot 32(8):852–854

    Article  CAS  PubMed  Google Scholar 

  • Feng Y, Shao Y, Chen F (2012) Monascus pigments. Appl Microbiol Biotechnol 96(6):1421–1440. doi:10.1007/s00253-012-4504-3

    Article  CAS  PubMed  Google Scholar 

  • GB 4926–2008: Food additive-red kojic rice (powder). ICS 67. 220. 20,X 41 (Chinese standard) General Administration of Quality Supervision, Inspection and Quarantine of the People’s Republic of China (AQSIQ) and Standardization Administration of the People’s Republic of China (SAC) on December 3, 2008

  • Hajjaj H, Klaébé A, Loret MO, Goma G, Blanc PJ, François J (1999) Biosynthetic pathway of citrinin in the filamentous fungus Monascus ruber as revealed by 13C nuclear magnetic resonance. Appl Environ Microbiol 65(1):311–314

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hajjaj H, Klaébé A, Goma G, Blanc PJ, Barbier E, François J (2000) Medium-chain fatty acids affect citrinin production in the filamentous fungus Monascus ruber. Appl Environ Microbiol 66(3):1120–1125. doi:10.1128/aem.66.3.1120-1125.2000

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • He Y, Liu Q, Shao Y, Chen F (2013) ku70 and ku80 null mutants improve the gene targeting frequency in Monascus ruber M7. Appl Microbiol Biotechnol 97(11):4965–4976. doi:10.1007/s00253-013-4851-8

    Article  CAS  PubMed  Google Scholar 

  • Hood E, Gelvin S, Melchers L, Hoekema A (1993) New Agrobacterium helper plasmids for gene transfer to plants. Transgenic Res 2(4):208–218. doi:10.1007/bf01977351

    Article  CAS  Google Scholar 

  • Huang C-H, Shiu S-M, Wu M-T, Chen W-L, Wang S-G, Lee H-M (2013) Monacolin-K affects lipid metabolism through SIRT1/AMPK pathway in HepG2 cells. Arch Pharm Res:1–11. doi:10.1007/s12272-013-0150-2

  • Hyndman D, Bauman DR, Heredia VV, Penning TM (2003) The aldo-keto reductase superfamily homepage. Chem Biol Interact 143–144:621–631. doi:10.1016/S0009-2797(02)00193-X

    Article  PubMed  Google Scholar 

  • Jez JM, Penning TM (2001) The aldo-keto reductase (AKR) superfamily: an update. Chem Biol Interact 130–132:499–525. doi:10.1016/S0009-2797(00)00295-7

    Article  PubMed  Google Scholar 

  • Johnson DN, Egner PA, Obrian G, Glassbrook N, Roebuck BD, Sutter TR, Payne GA, Kensler TW, Groopman JD (2008) Quantification of urinary aflatoxin B1 dialdehyde metabolites formed by aflatoxin aldehyde reductase using isotope dilution tandem mass spectrometry. Chem Res Toxicol 21(3):752–760. doi:10.1021/tx700397n

    Article  CAS  PubMed  Google Scholar 

  • Jongrungruangchok S, Kittakoop P, Yongsmith B, Bavovada R, Tanasupawat S, Lartpornmatulee N, Thebtaranonth Y (2004) Azaphilone pigments from a yellow mutant of the fungus Monascus kaoliang. Phytochemistry 65(18):2569–2575. doi:10.1016/j.phytochem.2004.08.032

    Article  CAS  PubMed  Google Scholar 

  • Judah DJ, Hayes JD, Yang JC, Lian LY, Roberts GC, Farmer PB, Lamb JH, Neal GE (1993) A novel aldehyde reductase with activity towards a metabolite of aflatoxin B1 is expressed in rat liver during carcinogenesis and following the administration of an anti-oxidant. Biochem J 292(1):13–18

    CAS  PubMed  Google Scholar 

  • Jůzlová P, Martínková L, KÅ™en V (1996) Secondary metabolites of the fungus Monascus: a review. J Ind Microbiol 16(3):163–170. doi:10.1007/bf01569999

    Article  Google Scholar 

  • Kelly Vincent P, O'Connor T, Ellis Elizabeth M, Ireland Linda S, Slattery Cara M, Sherratt Philip J, Crouch Dorothy H, Cavin C, Schilter B, Gallina A, Hayes John D (2003) Aflatoxin aldehyde reductases. Am Chem Soc 865(11):155–170

    Google Scholar 

  • Kim JH, Kim HJ, Kim C, Jung H, Kim YO, Ju JY, Shin CS (2007) Development of lipase inhibitors from various derivatives of monascus pigment produced by Monascus fermentation. Food Chem 101(1):357–364. doi:10.1016/j.foodchem.2005.11.055

    Article  CAS  Google Scholar 

  • Lee B-H, Pan T-M (2012a) Benefit of Monascus-fermented products for hypertension prevention: a review. Appl Microbiol Biotechnol 94(5):1151–1161. doi:10.1007/s00253-012-4076-2

    Article  CAS  PubMed  Google Scholar 

  • Lee C-L, Pan T-M (2012b) Development of Monascus fermentation technology for high hypolipidemic effect. Appl Microbiol Biotechnol 94(6):1449–1459. doi:10.1007/s00253-012-4083-3

    Article  CAS  PubMed  Google Scholar 

  • Lee C-L, Kung Y-H, Wu C-L, Hsu Y-W, Pan T-M (2010) Monascin and ankaflavin act as novel hypolipidemic and high-density lipoprotein cholesterol-raising agents in red mold Dioscorea. J Agric Food Chem 58(16):9013–9019. doi:10.1021/jf101982v

    Article  CAS  PubMed  Google Scholar 

  • Lin TF, Yakushijin K, Büchi GH, Demain AL (1992) Formation of water-soluble Monascus red pigments by biological and semi-synthetic processes. J Ind Microbiol 9(3–4):173–179. doi:10.1007/bf01569621

    Article  CAS  Google Scholar 

  • Lin Y-L, Wang T-H, Lee M-H, Su N-W (2008) Biologically active components and nutraceuticals in the Monascus-fermented rice: a review. Appl Microbiol Biotechnol 77(5):965–973. doi:10.1007/s00253-007-1256-6

    Article  CAS  PubMed  Google Scholar 

  • Mukherjee G, Singh SK (2011) Purification and characterization of a new red pigment from Monascus purpureus in submerged fermentation. Process Biochem 46(1):188–192. doi:10.1016/j.procbio.2010.08.006

    Article  CAS  Google Scholar 

  • Patakova P (2013) Monascus secondary metabolites: production and biological activity. J Ind Microbiol Biotechnol 40(2):169–181. doi:10.1007/s10295-012-1216-8

    Article  CAS  PubMed  Google Scholar 

  • Qu J (2008) Preliminary study on the function of pigment components isolated from Hongqu. (Master Thesis) Huazhong Agricultural University, Wuhan, Hubei, China

  • Shao Y, Ding Y, Zhao Y, Yang S, Xie B, Chen F (2009) Characteristic analysis of transformants in T-DNA mutation library of Monascus ruber. World J Microbiol Biotechnol 25(6):989–995. doi:10.1007/s11274-009-9977-6

    Article  CAS  Google Scholar 

  • Su Y-C, Wang J-J, Lin T-T, Pan T-M (2003) Production of the secondary metabolites γ-aminobutyric acid and monacolin K by Monascus. J Ind Microbiol Biotechnol 30(1):41–46. doi:10.1007/s10295-002-0001-5

    CAS  PubMed  Google Scholar 

  • Van Tieghem M (1884) Monascus, genre nouveau de l'ordre des Ascomycetes. Bull Soc Bot Fr 31:226–231

    Google Scholar 

  • Wang L, Wang W, Xu G (2011) Promotion of monacolin K production by Agrobacterium tumefaciens-mediated transformation in Monascus albidus 9901. Curr Microbiol 62(2):501–507. doi:10.1007/s00284-010-9735-x

    Article  CAS  PubMed  Google Scholar 

  • Xie N, Liu Q, Chen F (2013) Deletion of pigR gene in Monascus ruber leads to loss of pigment production. Biotechnol Lett 35(9):1425–1432. doi:10.1007/s10529-013-1219-1

    Article  CAS  PubMed  Google Scholar 

  • Yu Y, Du J, Wang G, Ji J (2003) Studies on the freeze-thaw method of transforming recombinant plasmid DNA into Agrobacterium tumefaciens. J Jilin Agric Univ 25:257–259, in Chinese

    Google Scholar 

  • Yu J-H, Hamari Z, Han K-H, Seo J-A, Reyes-Domínguez Y, Scazzocchio C (2004) Double-joint PCR: a PCR-based molecular tool for gene manipulations in filamentous fungi. Fungal Genet Biol 41(11):973–981. doi:10.1016/j.fgb.2004.08.001

    Article  CAS  PubMed  Google Scholar 

  • Zheng Y, Xin Y, Shi X, Guo Y (2010) Anti-cancer effect of rubropunctatin against human gastric carcinoma cells BGC-823. Appl Microbiol Biotechnol 88(5):1169–1177. doi:10.1007/s00253-010-2834-6

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was financially supported by the programs of the National Natural Science Foundation of China (no.31171649 and no.31271834).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Fusheng Chen.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Liu, Q., Xie, N., He, Y. et al. MpigE, a gene involved in pigment biosynthesis in Monascus ruber M7. Appl Microbiol Biotechnol 98, 285–296 (2014). https://doi.org/10.1007/s00253-013-5289-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-013-5289-8

Keywords

Navigation