Microarray analysis of p-anisaldehyde-induced transcriptome of Saccharomyces cerevisiae

  • Lu Yu
  • Na Guo
  • Yi Yang
  • Xiuping Wu
  • Rizeng Meng
  • Junwen Fan
  • Fa Ge
  • Xuelin Wang
  • Jingbo Liu
  • Xuming Deng
Original Paper

Abstract

p-Anisaldehyde (4-methoxybenzaldehyde), an extract from Pimpinella anisum L. seeds, is a potential novel preservative. To reveal the possible action mechanism of p-anisaldehyde against microorganisms, yeast-based commercial oligonucleotide microarrays were used to analyze the genome-wide transcriptional changes in response to p-anisaldehyde. Quantitative real-time RT-PCR was performed for selected genes to verify the microarray results. We interpreted our microarray data with the clustering tool, T-profiler. Analysis of microarray data revealed that p-anisaldehyde induced the expression of genes related to sulphur assimilation, aromatic aldehydes metabolism, and secondary metabolism, which demonstrated that the addition of p-anisaldehyde may influence the normal metabolism of aromatic aldehydes. This genome-wide transcriptomics approach revealed first insights into the response of Saccharomyces cerevisiae (S. cerevisiae) to p-anisaldehyde challenge.

Keywords

p-Anisaldehyde Antimicrobial Gene expression profile DNA microarray 

Notes

Acknowledgments

We are grateful to Dr. LiangZhang (CapitalBio) for oligonucleotide microarray analysis. This work was supported by the national basic research program (program 973) (2006CB504402).

Supplementary material

10295_2009_676_MOESM1_ESM.doc (1.5 mb)
(DOC 1.47 mb)

References

  1. 1.
    Beuchat LR, Golden DA (1989) Antimicrobials occurring naturally in foods. Food Technol 43:134–142Google Scholar
  2. 2.
    Lopez-Malo A, Alzamora SM, Argaiz A (1995) Effect of natural vanillin on germination time and radial growth of moulds in fruit-based agar systems. Food Mirobiol 12:213–219CrossRefGoogle Scholar
  3. 3.
    Cerrutti P, Alzamora SM (1996) Inhibitory effects of vanillin on some food spoilage yeasts in laboratory media and fruit purees. Int J Food Microbiol 29:379–386CrossRefPubMedGoogle Scholar
  4. 4.
    Fitzgerald DJ, Stratford M, Gasson MJ, Narbad A (2004) The potential application of vanillin in preventing yeast spoilage of soft drinks and fruit juices. J Food Prot 67:391–395PubMedGoogle Scholar
  5. 5.
    Fitzgerald DJ, Stratford M, Gasson MJ, Narbad A (2005) Structure-function analysis of the vanillin molecule and its antifungal properties. J Agric Food Chem 53:1769–1775CrossRefPubMedGoogle Scholar
  6. 6.
    Parveen M, Hasan MK, Takahashi J, Murata Y, Kitagawa E, Kodama O, Iwahashi H (2004) Response of Saccharomyces cerevisiae to a monoterpene: evaluation of antifungal potential by DNA microarray analysis. J Antimicrob Chemother 54:46–55CrossRefPubMedGoogle Scholar
  7. 7.
    Rojas M, Casado M, Portugal J, Piña B (2008) Selective inhibition of yeast regulons by daunorubicin: a transcriptome-wide analysis. BMC Genomics 30:358CrossRefGoogle Scholar
  8. 8.
    Rojas M, Wright CW, Piña B, Portugal J (2008) Genomewide expression profiling of cryptolepine-induced toxicity in Saccharomyces cerevisiae. Antimicrob Agents Chemother 52:3844–3850CrossRefPubMedGoogle Scholar
  9. 9.
    Goffeau A (2000) Four years of post-genomic life with 6, 000 yeast genes. FEBS Lett 480:37–41CrossRefPubMedGoogle Scholar
  10. 10.
    National Committee for Clinical Laboratory Standards (NCCLS) (1997) Reference method for broth dilution antifungal susceptibility testing of yeasts. proposed standard M27-A. National Committee for Clinical Laboratory Standards, VillanovaGoogle Scholar
  11. 11.
    Zhang W, Needham DL, Coffin M, Rooker A, Hurban P, Tanzer MM, Shuster JR (2003) Microarray analyses of the metabolic responses of Saccharomyces cerevisiae to organic solvent dimethyl sulfoxide. J Ind Microbiol Biotechnol 30:57–69PubMedGoogle Scholar
  12. 12.
    Collart MA, Oliviero S (1995) Preparation of yeast RNA. Short protocols in molecular biology, 3rd edn. Wiley, New York, pp 1346–1347Google Scholar
  13. 13.
    Guo Y, Guo H, Zhang L (2005) Genomic analysis of anti-hepatitis B virus (HBV) activity by small interfering RNA and lamivudine in stable HBV-producing cells. J Virol 79:14392–14403CrossRefPubMedGoogle Scholar
  14. 14.
    Yang YH, Dudoit S, Luu P, Lin DM, Peng V, Ngai J, Speed TP (2002) Normalization for cDNA microarray data: a robust composite method addressing single and multiple slide systematic variation. Nucleic Acids Res 30:e15CrossRefPubMedGoogle Scholar
  15. 15.
    Wai-Leung Ng, Kazmierczak KM, Robertson GT, Gilmour R, Winkler ME (2003) Transcriptional regulation and signature patterns revealed by microarray analyses of Streptococcus pneumoniae R6 challenged with sublethal concentrations of translation inhibitors. J Bacteriol 185:359–370CrossRefGoogle Scholar
  16. 16.
    Boorsma A, Foat BC, Vis D, Klis F, Bussemaker HJ (2005) T-profiler: scoring the activity of predefined groups of genes using gene expression data. Nucleic Acids Res 33:W592–W595CrossRefPubMedGoogle Scholar
  17. 17.
    Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G (2000) Gene ontology: tool for the unification of biology. the gene ontology consortium. Nat Genet 25:25–29CrossRefPubMedGoogle Scholar
  18. 18.
    Zakrzewska A, Boorsma A, Delneri D, Stanley B, Oliver SB, Klis FM (2007) Cellular processes and pathways that protect Saccharomyces cerevisiae cells against the plasma membrane-perturbing compound chitosan. Eukaryot Cell 6:600–608CrossRefPubMedGoogle Scholar
  19. 19.
    Nakamura K, Niimi M, Niimi K, Holmes AR, Yates JE, Decottignies A, Monk BC, Goffeau A, Cannon RD (2001) Functional expression of Candida albicans drug efflux pump cdr1p in a Saccharomyces cerevisiae strain deficient in membrane transporters. Antimicrob Agents Chemother 45:3366–3374CrossRefPubMedGoogle Scholar
  20. 20.
    Regenberg B, Grotkjaer T, Winther O, Fausbøll A, Åkesson M, Bro C, Hansen LK, Brunak S, Nielsen J (2006) Growth-rate regulated genes have profound impact on interpretation of transcriptome profiling in Saccharomyces cerevisiae. Genome Biol 7:R107CrossRefPubMedGoogle Scholar
  21. 21.
    Causton HC, Ren B, Koh SS, Harbison CT, Kanin E, Jennings EG, Lee TI, True HL, Lander ES, Young RA (2001) Remodeling of yeast genome expression in response to environmental changes. Mol Biol Cell 12:323–337PubMedGoogle Scholar
  22. 22.
    Gasch AP, Spellman PT, Kao CM, Carmel-Harel O, Eisen MB, Storz G, Botstein D, Brown PO (2000) Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell 11:4241–4257PubMedGoogle Scholar
  23. 23.
    Bro C, Regenberg B, Lagniel G, Labarre J, Montero-Lomeli M, Nielsen J (2003) Transcriptional, proteomic, and metabolic responses to lithium in galactose-grown yeast cells. J Biol Chem 278:32141–32149CrossRefPubMedGoogle Scholar
  24. 24.
    Hardwick JS, Kuruvilla FG, Tong JK, Shamji AF, Schreiber SL (1999) Rapamycin-modulated transcription defines the subset of nutrient-sensitive signaling pathways directly controlled by the TOR proteins. Proc Natl Acad Sci 96:14866–14870CrossRefPubMedGoogle Scholar
  25. 25.
    Schuurmans JM, Boorsma A, Lascaris R, Hellingwerf KJ (2008) Teixeira de Mattos MJ physiological and transcriptional characterization of Saccharomyces cerevisiae strains with modifed expression of catabolic regulators. FEMS Yeast Res 8:26–34CrossRefPubMedGoogle Scholar
  26. 26.
    Bammert GF, Fostel JM (2000) Genome-wide expression patterns in Saccharomyces cerevisiae: comparison of drug treatments and genetic alterations affecting biosynthesis of ergosterol. Antimicro Agents Chemother 44:1255–1265CrossRefGoogle Scholar
  27. 27.
    Cavalieri D, Townsend JP, Hartl DL (2000) Manifold anomalies in gene expression in a vineyard isolate of Saccharomyces cerevisiae revealed by DNA microarray analysis. PNAS 97:12369–12374CrossRefPubMedGoogle Scholar
  28. 28.
    Aranda A, del Olmo M (2004) Exposure of Saccharomyces cerevisiae to acetaldehyde induces sulfur amino acid metabolism and polyamine transporter genes, which depend on Met4p and Haa1p transcription factors, respectively. Appl Environ Microbiol 70:1913–1922CrossRefPubMedGoogle Scholar
  29. 29.
    Thomas D, Surdin-Kerjan Y (1997) Metabolism of sulfur amino acids in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 61:503–532PubMedGoogle Scholar
  30. 30.
    Delneri D, Gardner DC, Bruschi CV, Oliver SG (1999) Disruption of seven hypothetical aryl alcohol dehydrogenase genes from Saccharomyces cerevisiae and construction of a multiple knock-out strain. Yeast 15:1681–1689CrossRefPubMedGoogle Scholar
  31. 31.
    Delneri D, Gardner DC, Oliver SG (1999) Analysis of the seven member AAD gene set demonstrates that genetic redundancy in yeast may be more apparent than real. Genetics 153:1591–1600PubMedGoogle Scholar
  32. 32.
    Kitagawa E, Momose Y, Iwahashi H (2003) Correlation of the structures of agricultural fungicides to gene expression in Saccharomyces cerevisiae upon exposure to toxic doses. Environ Sci Technol 37:2788–9273CrossRefPubMedGoogle Scholar
  33. 33.
    Agarwal AK, Rogers PD, Baerson SR, Jacob MR, Barker KS, Cleary JD, Walker LA, Nagle DG, Clark AM (2003) Genome-wide expression profiling of the response to polyene, pyrimidine, azole, and echinocandin antifungal agents in Saccharomyces cerevisiae. J Biol Chem 278:34998–35015CrossRefPubMedGoogle Scholar
  34. 34.
    Zakrzewska A, Boorsma A, Brul S, Hellingwerf KJ, Klis FM (2005) Transcriptional response of Saccharomyces cerevisiae to the plasma membrane-perturbing compound chitosan. Eukaryot Cell 4:703–715CrossRefPubMedGoogle Scholar
  35. 35.
    Jamieson DJ (1992) Saccharomyces cerevisiae has distinct adaptive responses to both hydrogen peroxide and menadione. J Bacteriol 174:6678–6681PubMedGoogle Scholar
  36. 36.
    Collinson LP, Dawes IW (1992) Inducibility of the response of yeast cells to peroxide stress. J Gen Microbiol 138:329–335PubMedGoogle Scholar
  37. 37.
    Stephen DWS, Rivers SL, Jamieson DJ (1995) The role of the Yap1 and Yap2 genes in the regulation of the adaptive oxidative stress responses of Saccharomyces cerevisiae. Mol Microbiol 16:415–423CrossRefPubMedGoogle Scholar
  38. 38.
    Fishman-Lobell J, Rudin N, Haber JE (1992) Two alternative pathways of double-strand break repair that are kinetically separable and independently modulated. Mol Cell Biol 12:1292–1302PubMedGoogle Scholar
  39. 39.
    van den Bosch M, Zonneveld JB, Vreeken K, de Vries FA, Lohman PH, Pastink A (2002) Differential expression and requirements for Schizosaccharomyces pombe RAD52 homologs in DNA repair and recombination. Nucleic Acids Res 30:1316–1324CrossRefPubMedGoogle Scholar
  40. 40.
    Ohta T (1993) Modification of genotoxicity by naturally occurring favorings and their derivatives. Crit Rev Toxicol 23:127–146CrossRefPubMedGoogle Scholar
  41. 41.
    Akagi K, Hirose M, Hoshiya T, Mizoguchi Y, Ito N, Shirai T (1995) Modulating effects of elagic acid, vanillin and quercetin in a rat medium term multi-organ carcinogenesis model. Cancer Lett 94:113–121CrossRefPubMedGoogle Scholar
  42. 42.
    Lord CJ, Garrett MD, Ashworth A (2006) Targeting the double-strand DNA break repair pathway as a therapeutic strategy. Clin Cancer Res 12:4463–4468CrossRefPubMedGoogle Scholar
  43. 43.
    Tamai K, Tezuka H, Kuroda Y (1992) Direct modifications by vanillin in cytotoxicity and genetic changes induced by EMS and H2O2 in cultured chinese hamster cells. Mutat Res 268:231–237PubMedGoogle Scholar
  44. 44.
    Gustafson DL, Franz HR, Ueno AM, Smith CJ, Doolittle DJ, Waldren CA (2000) Vanillin (3-methoxy-4-hydroxybenzaldehyde) inhibits mutation induced by hydrogen peroxide, N-methyl-N-nitrosoguanidine and mitomycin C but not (137)Cs gamma-radiation at the CD59 locus in human-hamster hybrid A(L) cells. Mutagenesis 15:207–213CrossRefPubMedGoogle Scholar
  45. 45.
    Balzi E, Goffeau A (1995) Yeast multidrug resistance: the PDR network. J Bioenerg Biomembr 27:71–76CrossRefPubMedGoogle Scholar
  46. 46.
    Decottignies A, Grant AM, Nichols JW, de Wet H, McIntosh DB, Goffeau A (1998) ATPase and multidrug transport activities of the overexpressed yeast ABC protein Yor1p. J Biol Chem 273:12612–12622CrossRefPubMedGoogle Scholar
  47. 47.
    Katzmann DJ, Burnett PE, Golin J, Mahé Y (1994) Moye-Rowley WS Transcriptional control of the yeast PDR5 gene by the PDR3 gene product. Mol Cell Biol 14:4653–4661PubMedGoogle Scholar
  48. 48.
    Owsianik G, Balzi L, Ghislain M (2002) Control of 26S proteasome expression by transcription factors regulating multidrug resistance in Saccharomyces cerevisiae. Mol Microbiol 43:1295–1308CrossRefPubMedGoogle Scholar
  49. 49.
    Teixeira MC, Dias PJ, Simões T (2008) Sá-Correia I Yeast adaptation to mancozeb involves the up-regulation of FLR1 under the coordinate control of Yap1, Rpn4, Pdr3, and Yrr1. Biochem Biophys Res Commun 367:249–255CrossRefPubMedGoogle Scholar
  50. 50.
    Fan X, Shi H, Lis JT (2005) Distinct transcriptional responses of RNA polymerases I, II and III to aptamers that bind TBP. Nucleic Acids Res 33:838–845CrossRefPubMedGoogle Scholar
  51. 51.
    Koch C, Moll T, Neuberg M, Ahorn H, Nasmyth K (1993) A role for the transcription factors Mbp1 and Swi4 I progression from G1 to S phase. Science 261:1551–1557CrossRefPubMedGoogle Scholar
  52. 52.
    Bean JM, Siggia ED, Cross FR (2005) High functional overlap between MluI cell-cycle box binding factor and Swi4/6 cell-cycle box binding factor in the G1/S transcriptional program in Saccharomyces cerevisiae. Genetics 171:49–61CrossRefPubMedGoogle Scholar
  53. 53.
    Jorgensen P, Nishikawa JL, Breitkreutz BJ, Tyers M (2002) Systematic identification of pathways that couple cell growth and division in yeast. Science 297:395–400CrossRefPubMedGoogle Scholar
  54. 54.
    Toone WM, Aerne BL, Morgan BA, Johnston LH (1997) Getting started: regulating the initiation of DNA replication in yeast. Annu Rev Microbiol 51:125–149CrossRefPubMedGoogle Scholar
  55. 55.
    Koranda M, Schleiffer A, Endler L, Ammerer G (2000) Forkhead-like transcription factors recruit Ndd1 to the chromatin of G2/M-specific promoters. Nature 406:94–98CrossRefPubMedGoogle Scholar
  56. 56.
    Hollenhorst PC, Bose ME, Mielke MR, Muller U, Fox CA (2000) Forkhead genes in transcriptional silencing, cell morphology and the cell cycle. overlapping and distinct functions for FKH1 and FKH2 in Saccharomyces cerevisiae. Genetics 154:1533–1548PubMedGoogle Scholar
  57. 57.
    Spellman PT, Sherlock G, Zhang MQ, Iyer VR, Anders K (1998) Comprehensive identification of cell-cycle regulated genes of the yeast Saccharomyces cerevisiae by microarray hybridization. Mol Biol Cell 9:3273–3297PubMedGoogle Scholar
  58. 58.
    Veis J, Klug H, Koranda M, Ammerer G (2007) Activation of the G2/M-specific gene CLB2 requires multiple cell cycle signals. Mol Cell Biol 27:8364–8373CrossRefPubMedGoogle Scholar
  59. 59.
    Zhu G, Spellman PT, Volpe T, Brown PO, Botstein D, Davis TN, Futcher B (2000) Two yeast forkhead genes regulate the cell cycle and pseudohyphal growth. Nature 406:90–94CrossRefPubMedGoogle Scholar
  60. 60.
    Lu L, Roberts G, Simon K, Yu J, Hudson AP (2003) Rsf1p, a protein required for respiratory growth of Saccharomyces cerevisiae. Curr Genet 43:263–272CrossRefPubMedGoogle Scholar

Copyright information

© Society for Industrial Microbiology 2009

Authors and Affiliations

  • Lu Yu
    • 1
  • Na Guo
    • 1
    • 2
  • Yi Yang
    • 1
  • Xiuping Wu
    • 1
  • Rizeng Meng
    • 3
  • Junwen Fan
    • 4
  • Fa Ge
    • 1
  • Xuelin Wang
    • 1
  • Jingbo Liu
    • 2
  • Xuming Deng
    • 1
  1. 1.Key Laboratory of Zoonosis, Ministry of Education, Institute of Zoonosis, College of Animal Science and Veterinary MedicineJilin UniversityChangchunChina
  2. 2.Laboratory of Nutrition and Functional FoodJilin UniversityChangchunChina
  3. 3.Jilin Enrty-exit Inspection and Quarantine BureauChangchunChina
  4. 4.Laboratory Animal CenterAcademy of Military Medical SciencesBeijingChina

Personalised recommendations