Engineering of synthetic, stress-responsive yeast promoters

Nucleic Acids Research

Volumn 44, Issue 17, 2016, Pages

  Rajkumar, Arun S ^a   Liu, Guodong ^b   Bergenholm, David ^b   Arsovska, Dushica ^a   Kristensen, Mette ^a   Nielsen, Jens ^a,b   Jensen, Michael K ^a   Keasling, Jay D ^a,c,d,e  

^a Chalmers University of Technology   (Denmark)

^b CHALMERS UNIVERSITY OF TECHNOLOGY   (Sweden)

^c JOINT BIOENERGY INSTITUTE   (United States)

^d LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BINDING SITE; CCW14 GENE; CONTROLLED STUDY; FERMENTATION TECHNIQUE; FUNGAL GENE; GENE SEQUENCE; GENETIC ENGINEERING; METABOLIC ENGINEERING; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; SACCHAROMYCES CEREVISIAE; SEQUENCE ANALYSIS; TEF1 GENE; TRANSCRIPTION REGULATION; YEAST; YGP1 GENE; FERMENTATION; FLUORESCENCE; GENETICS; METABOLISM; PH; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PROCEDURES; SYNTHETIC BIOLOGY;

LACTIC ACID; MESSENGER RNA; SACCHAROMYCES CEREVISIAE PROTEIN; TRANSCRIPTION FACTOR;

BINDING SITES; FERMENTATION; FLUORESCENCE; GENETIC ENGINEERING; HYDROGEN-ION CONCENTRATION; LACTIC ACID; PROMOTER REGIONS, GENETIC; RNA, MESSENGER; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; STRESS, PHYSIOLOGICAL; SYNTHETIC BIOLOGY; TRANSCRIPTION FACTORS;

EID: 84991225926     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkw553     Document Type: Article

References (57)

1. Keasling, J.D. (2012) Synthetic biology and the development of tools for metabolic engineering. Metab. Eng., 14, 189-195.
2. Paddon, C.J., Westfall, P.J., Pitera, D.J., Benjamin, K., Fisher, K., McPhee, D., Leavell, M.D., Tai, A., Main, A., Eng, D. et al. (2013) High-level semi-synthetic production of the potent antimalarial artemisinin. Nature, 496, 528-532.
3. Brown, S., Clastre, M., Courdavault, V. and O'Connor, S.E. (2015) De novo production of the plant-derived alkaloid strictosidine in yeast. Proc. Natl. Acad. Sci. U.S.A., 112, 3205-3210.
4. Jeppsson, M., Johansson, B., Jensen, P.R., Hahn-Hägerdal, B. and Gorwa-Grauslund, M.F. (2003) The level of glucose-6-phosphate dehydrogenase activity strongly influences xylose fermentation and inhibitor sensitivity in recombinant Saccharomyces cerevisiae strains. Yeast, 20, 1263-1272.
5. Blount, B.A., Weenink, T., Vasylechko, S. and Ellis, T. (2012) Rational diversification of a promoter providing fine-tuned expression and orthogonal regulation for synthetic biology. PLoS One, 7, 1-11.
6. Blazeck, J., Garg, R., Reed, B. and Alper, H.S. (2012) Controlling promoter strength and regulation in Saccharomyces cerevisiae using synthetic hybrid promoters. Biotechnol. Bioeng., 109, 2884-2895.
7. Curran, K.A., Crook, N.C., Karim, A.S., Gupta, A., Wagman, A.M. and Alper, H.S. (2014) Design of synthetic yeast promoters via tuning of nucleosome architecture. Nat. Commun., 5, 4002.
8. Redden, H. and Alper, H.S. (2015) The development and characterization of synthetic minimal yeast promoters. Nat. Commun., 6, 7810.
9. Cao, L., Tang, X., Zhang, X., Zhang, J., Tian, X., Wang, J., Xiong, M. and Xiao, W. (2014) Two-stage transcriptional reprogramming in Saccharomyces cerevisiae for optimizing ethanol production from xylose. Metab. Eng., 24, 150-159.
10. Dahl, R.H., Zhang, F., Alonso-Gutierrez, J., Baidoo, E., Batth, T.S., Redding-Johanson, A.M., Petzold, C.J., Mukhopadhyay, A., Lee, T.S., Adams, P.D. et al. (2013) Engineering dynamic pathway regulation using stress-response promoters. Nat. Biotechnol., 31, 1039-1046.
11. Yuan, J. and Ching, C.B. (2015) Dynamic control of ERG9 expression for improved amorpha-4, 11-diene production in Saccharomyces cerevisiae. Microb. Cell Fact., 14, 1-10.
12. Abbott, D.A., Zelle, R.M., Pronk, J.T. and Van Maris, A.J.A. (2009) Metabolic engineering of Saccharomyces cerevisiae for production of carboxylic acids: Current status and challenges. FEMS Yeast Res., 9, 1123-1136.
13. Jensen, N.B., Strucko, T., Kildegaard, K.R., David, F., Maury, J., Mortensen, U.H., Forster, J., Nielsen, J. and Borodina, I. (2014) EasyClone: method for iterative chromosomal integration of multiple genes in Saccharomyces cerevisiae. FEMS Yeast Res., 14, 238-248.
14. Nijkamp, J.F., van den Broek, M., Datema, E., de Kok, S., Bosman, L., Luttik, M.A., Daran-Lapujade, P., Vongsangnak, W., Nielsen, J., Heijne, W.H. et al. (2012) De novo sequencing, assembly and analysis of the genome of the laboratory strain Saccharomyces cerevisiae CEN.PK113-7D, a model for modern industrial biotechnology. Microb. Cell Fact., 11, 36.
15. MacIsaac, K.D., Wang, T., Gordon, D.B., Gifford, D.K., Stormo, G.D. and Fraenkel, E. (2006) An improved map of conserved regulatory sites for Saccharomyces cerevisiae. BMC Bioinformatics, 7, 113.
16. De Boer, C.G. and Hughes, T.R. (2012) YeTFaSCo: a database of evaluated yeast transcription factor sequence specificities. Nucleic Acids Res., 40, D169-D179.
17. Badis, G., Chan, E.T., van Bakel, H., Pena-Castillo, L., Tillo, D., Tsui, K., Carlson, C.D., Gossett, A.J., Hasinoff, M.J., Warren, C.L. et al. (2008) A library of yeast transcription factor motifs reveals a widespread function for Rsc3 in targeting nucleosome exclusion at promoters. Mol. Cell, 32, 878-887.
18. Jung, U.S. and Levin, D.E. (1999) Genome-wide analysis of gene expression regulated by the yeast cell wall integrity signalling pathway. Mol. Microbiol., 34, 1049-1057.
19. Mira, N.P., Henriques, S.F., Keller, G., Teixeira, M.C., Matos, R.G., Arraiano, C.M., Winge, D.R. and Sá-Correia, I. (2011) Identification of a DNA-binding site for the transcription factor Haa1, required for Saccharomyces cerevisiae response to acetic acid stress. Nucleic Acids Res., 39, 6896-6907.
20. Boulet-Eckert, N., Pedersen, M.L., Krogh, B.O. and Lisby, M. (2012) Optimization of ordered plasmid assembly by gap repair in Saccharomyces cerevisiae. Yeast, 29, 323-334.
21. Gietz, R.D. and Schiestl, R.H. (2007) High-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method. Nat. Protoc., 2, 31-34.
22. Stovicek, V., Borodina, I. and Forster, J. (2015) CRISPR-Cas system enables fast and simple genome editing of industrial Saccharomyces cerevisiae strains. Metab. Eng. Commun., 2, 13-22.
23. Lee, S., Lim, W.A. and Thorn, K.S. (2013) Improved blue, green, and red fluorescent protein tagging vectors for S. cerevisiae. PLoS One, 8, e67902.
24. Jakociunas, T., Rajkumar, A.S., Zhang, J., Arsovska, D., Rodriguez, A., Jendresen, C.B., Skjoedt, M.L., Nielsen, A.T., Borodina, I., Jensen, M.K. et al. (2015) CasEMBLR: Cas9-facilitated multi-loci genomic integration of in vivo assembled DNA parts in Saccharomyces cerevisiae. ACS Synth. Biol., 4, 1226-1234.
25. Hamilton, R., Watanabe, C.K. and de Boer, H.A. (1987) Compilation and comparison of the sequence context around the AUG startcodons in Saccharomyces cerevisiae mRNAs. Nucleic Acids Res., 15, 3581-3593.
26. Shao, Z., Zhao, H. and Zhao, H. (2009) DNA assembler, an in vivo genetic method for rapid construction of biochemical pathways. Nucleic Acids Res., 37, 1-10.
27. Kildegaard, K.R., Hallström, B.M., Blicher, T.H., Sonnenschein, N., Jensen, N.B., Sherstyk, S., Harrison, S.J., Maury, J., Herrgård, M.J., Juncker, A.S. et al. (2014) Evolution reveals a glutathione-dependent mechanism of 3-hydroxypropionic acid tolerance. Metab. Eng., 26, 57-66.
28. De Lucena, R.M., Elsztein, C., Simões, D.A. and De Morais, M.A. Jr (2012) Participation of CWI, HOG and Calcineurin pathways in the tolerance of Saccharomyces cerevisiae to low pH by inorganic acid. J. Appl. Microbiol., 113, 629-640.
29. Zuker, M. (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res., 31, 3406-3415.
30. Muller, P.Y., Janovjak, H., Miserez, A.R. and Dobbie, Z. (2002) Processing of gene expression data generated by quantitative real-time RT-PCR. Biotechniques, 32, 1372-1379.
31. Janke, C., Magiera, M.M., Rathfelder, N., Taxis, C., Reber, S., Maekawa, H., Moreno-Borchart, A., Doenges, G., Schwob, E., Schiebel, E. et al. (2004) A versatile toolbox for PCR-based tagging of yeast genes: New fluorescent proteins, more markers and promoter substitution cassettes. Yeast, 21, 947-962.
32. Van Driessche, B., Tafforeau, L., Hentges, P., Carr, A.M. and Vandenhaute, J. (2005) Additional vectors for PCR-based gene tagging in Saccharomyces cerevisiae and Schizosaccharomyces pombe using nourseothricin resistance. Yeast, 22, 1061-1068.
33. Liu, G., Bergenholm, D. and Nielsen, J. (2016) Genome-wide mapping of binding sites reveals multiple biological functions of the transcription factor Cst6p in Saccharomyces cerevisiae. MBio, 7, 1-10.
34. Rhee, H.S. and Pugh, B.F. (2012) ChiP-exo method for identifying genomic location of DNA-binding proteins with near-single-nucleotide accuracy. Curr. Protoc. Mol. Biol., 100, 1-14.
35. Livak, K.J. and Schmittgen, T.D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-CT) method. Methods, 25, 402-408.
36. Kapteyn, J.C., Ter Riet, B., Vink, E., Blad, S., De Nobel, H., Van Den Ende, H. and Klis, F.M. (2001) Low external pH induces HOG1-dependent changes in the organization of the Saccharomyces cerevisiae cell wall. Mol. Microbiol., 39, 469-479.
37. Kawahata, M., Masaki, K., Fujii, T. and Iefuji, H. (2006) Yeast genes involved in response to lactic acid and acetic acid: Acidic conditions caused by the organic acids in Saccharomyces cerevisiae cultures induce expression of intracellular metal metabolism genes regulated by Aft1p. FEMS Yeast Res., 6, 924-936.
38. De Melo, H.F., Bonini, B.M., Thevelein, J., Simões, D.A. and Morais, M.A. Jr (2010) Physiological and molecular analysis of the stress response of Saccharomyces cerevisiae imposed by strong inorganic acid with implication to industrial fermentations. J. Appl. Microbiol., 109, 116-127.
39. De Lucena, R.M., Elsztein, C., de Barros Pita, W., de Souza, R.B., de Sá Leitão Paiva, J.S. and de Morais, M.A. Jr (2015) Transcriptomic response of Saccharomyces cerevisiae for its adaptation to sulphuric acid-induced stress. Antonie Van Leeuwenhoek, 108, 1147-1160.
40. Carmelo, V. and Sá-Correia, I. (1997) HySP26 gene transcription is strongly induced during Saccharomyces cerevisiae growth at low pH. FEMS Microbiol. Lett., 149, 85-88.
41. Destruelle, M., Holzer, H. and Klionsky, D.J. (1994) Identification and characterization of a novel yeast gene: the YGP1 gene product is a highly glycosylated secreted protein that is synthesized in response to nutrient limitation. Mol. Cell. Biol., 14, 2740-2754.
42. Fernandes, A.R., Mira, N.P., Vargas, R.C., Canelhas, I. and Sá-Correia, I. (2005) Saccharomyces cerevisiae adaptation to weak acids involves the transcription factor Haa1p and Haa1p-regulated genes. Biochem. Biophys. Res. Commun., 337, 95-103.
43. Gatti, X., De Bettignies, G., Claret, S., Doignon, F., Crouzet, M. and Thoraval, D. (2005) RGD1, encoding a RhoGAP involved in low-pH survival, is an Msn2p/Msn4p regulated gene in Saccharomyces cerevisiae. Gene, 351, 159-169.
44. Claret, S., Gatti, X., Thoraval, D. and Crouzet, M. (2005) The Rgd1p Rho GTPase-activating protein and the Mid2p cell wall sensor are required at low pH for protein kinase C pathway activation and cell survival Eukaryot. Cell, 4, 1375-1386.
45. Levin, D.E. (2011) Regulation of cell wall biogenesis in Saccharomyces cerevisiae: the cell wall integrity signaling pathway. Genetics, 189, 1145-1175.
46. Ariño, J. (2010) Integrative responses to high pH stress in S. cerevisiae. OMICS, 14, 517-523.
47. Bitter, G.A., Chang, K.K. and Egan, K.M. (1991) A multi-component upstream activation sequence of the Saccharomyces cerevisiae glyceraldehyde-3-phosphate dehydrogenase gene promoter. Mol. Gen. Genet., 231, 22-32.
48. Fordyce, P.M., Gerber, D., Tran, D., Zheng, J., Li, H., DeRisi, J.L. and Quake, S.R. (2010) De novo identification and biophysical characterization of transcription-factor binding sites with microfluidic affinity analysis. Nat. Biotechnol., 28, 970-975.
49. Haase, S.B. and Wittenberg, C. (2014) Topology and control of the cell-cycle-regulated transcriptional circuitry. Genetics, 196, 65-90.
50. Sharon, E., Kalma, Y., Sharp, A., Raveh-Sadka, T., Levo, M., Zeevi, D., Keren, L., Yakhini, Z., Weinberger, A. and Segal, E. (2012) Inferring gene regulatory logic from high-throughput measurements of thousands of systematically designed promoters. Nat. Biotechnol., 30, 521-530.
51. Raveh-Sadka, T., Levo, M., Shabi, U., Shany, B., Keren, L., Lotan-Pompan, M., Zeevi, D., Sharon, E., Weinberger, A. and Segal, E. (2012) Manipulating nucleosome disfavoring sequences allows fine-tune regulation of gene expression in yeast. Nat. Genet., 44, 743-750.
52. Boorsma, A., De Nobel, H, Ter Riet, B., Bargmann, B., Brul, S., Hellingwerf, K.J. and Klis, F.M. (2004) Characterization of the transcriptional response to cell wall stress in Saccharomyces cerevisiae. Yeast, 21, 413-427.
53. Lawrence, C.L., Botting, C.H., Antrobus, R. and Coote, P.J. (2004) Evidence of a new role for the high-osmolarity glycerol mitogen-activated protein kinase pathway in yeast: regulating adaptation to citric acid stress evidence of a new role for the high-osmolarity glycerol mitogen-activated protein kinase pathway in yeast. Mol. Cell. Biol., 24, 3307-3324.
54. Venters, B.J., Wachi, S., Mavrich, T.N., Andersen, B.E., Jena, P., Sinnamon, A.J., Jain, P., Rolleri, N.S., Jiang, C., Hemeryck-Walsh, C. et al. (2011) A comprehensive genomic binding map of gene and chromatin regulatory proteins in Saccharomyces. Mol. Cell, 41, 480-492.
55. Ishida, N., Saitoh, S., Onishi, T., Tokuhiro, K., Nagamori, E., Kitamoto, K. and Takahashi, H. (2006) The effect of pyruvate decarboxylase gene knockout in Saccharomyces cerevisiae on L-lactic acid production. Biosci. Biotechnol. Biochem., 70, 1148-1153.
56. Leavitt, J.M. and Alper, H.S. (2015) Advances and current limitations in transcript-level control of gene expression. Curr. Opin. Biotechnol., 34, 98-104.
57. Nugroho, R.H., Yoshikawa, K. and Shimizu, H. (2015) Metabolomic analysis of acid stress response in Saccharomyces cerevisiae. J. Biosci. Bioeng., 120, 396-404.