Research Article
BibTex RIS Cite

THE SAGA COMPLEX IS ESSENTIAL FOR THE REGULATION OF GENES INVOLVED IN YEAST TREHALOSE METABOLISM

Year 2022, , 167 - 176, 15.10.2022

Tulay Turgut Genc

https://doi.org/10.23902/trkjnat.1131400
Cited By: 1

Abstract

Saccharomyces cerevisiae accumulates trehalose as a stress metabolite in adverse environmental conditions. The trehalose synthesis and breakdown are important for the regulation of trehalose levels within the yeast cell. Therefore, TPS1 and NTH1 gene expressions are tightly regulated during transcription and also translation. Since both genes contain Stress Response Elements (STRE) in the promoter regions, they are co-activated under stress conditions. However, the presence of similar regulatory elements in the promoter of both genes shows that these genes undergo a different regulation at the transcriptional level. In our study, the role of the Spt-Ada-Gcn5 Acetyltransferase (SAGA) complex in the transcriptional regulation of TPS1 and NTH1 genes was determined in nutrient-poor environment. For that purpose, the wild type and Δada1 mutant yeast cells, where Ada1p is a member of the SAGA complex, were grown in normal and nitrogen starvation conditions. In addition, trehalose level was detected enzymatically in both wild type and mutant yeast cells. In silico promoter analysis of TPS1 and NTH1 promoters revealed that the STRE sequences required for binding of Msn2/4 transcription factors are closed by nucleosomes at the NTH1 promoter, but open at the TPS1 promoter. In the absence of Ada1p, stress-induced promoter activation in the TPS1 gene was observed, while NTH1 gene expression was not activated. According to these results, the nucleosomes spanning the STRE sequences could not be mobilized in the absence of Ada1 protein, and therefore the Msn2/4 transcription factors cannot bind to the promoter and activate the NTH1 gene expression under stress conditions. It was also observed that in the absence of Ada1p, trehalose accumulation was reduced regardless of stress conditions. 

Keywords

Msn2/4 Nitrogen starvation Nucleosome SAGA Trehalose

Thanks

The author is grateful to Professor Jean Marie François (Institut National Des Sciences Appliquées, Toulouse, France) for the gift of LacZ fusion systems.

References

  • 1. Antonazzi, F., Di Felice, F. & Camilloni, G. 2021. GCN5 enables HSP12 induction promoting chromatin remodeling, not histone acetylation. Biochemistry and Cell Biology, 99(6): 700-706.
  • 2. App, H. & Holzer, H. 1989. Purification and characterization of neutral trehalase from the yeast ABYS1 mutant. Journal of Biological Chemistry, 264(29): 17583-17588.
  • 3. Arslan, M., Holyavkin, C., Kısakesen, H.İ., Topaloğlu, H.İ., Sürmeli, Y. & Çakar, Z.P. 2018. Physiological and transcriptomic analysis of a chronologically long-lived Saccharomyces cerevisiae strain obtained by evolutionary engineering. Molecular Biotechnology, 60: 468-484.
  • 4. Asada, R., Watanabe, T., Tanaka, Y., Kishida, M. & Furuta, M. 2022. Trehalose accumulation and radiation resistance due to prior heat stress in Saccharomyces cerevisiae. Archives of Microbiology, 204(5): 275.
  • 5. Ausubel, S.M., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A. & Struhl, K. 1993. Basic techniques of yeast genetics, pp 13.7.1-13.7.2. In: Ausubel, S.M., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A. & Struhl, K. (eds). Current Protocols in Molecular Biology, John Wiley & Sons, Inc., New York, 29B.3.22 pp.
  • 6. Balaban, B.G., Yılmaz, Ü., Alkım, C., Topaloğlu, A., Kısakesen, H.İ., Holyavkin, C. & Çakar, Z.P. 2019. Evolutionary engineering of an iron-resistant Saccharomyces cerevisiae mutant and its physiological and molecular characterization. Microorganisms, 8(1): 43.
  • 7. Beck, T. & Hall, M.N. 1999. The TOR signalling pathway controls nuclear localization of nutrient-regulated transcription factors. Nature, 402: 689-692.
  • 8. Bell, W., Sun, W., Hohmann, S., Wera, S., Reinders, A., De Virgilio, C. & Wiemken, A. 1998. Composition and functional analysis of the Saccharomyces cerevisiae trehalose synthase complex. Journal of Biological Chemistry, 273(50): 33311-33319.
  • 9. Belotserkovskaya, R., Sterner, D.E., Deng, M., Sayre, M.H., Lieberman, P.M. & Berger, S.L. 2000. Inhibition of TATA-binding protein function by SAGA subunits Spt3 and Spt8 at Gcn4-activated promoters. Molecular and Cellular Biology, 20(2): 634-647.
  • 10. Boeger, H., Griesenbeck, J., Strattan, J.S. & Kornberg, R.D. 2004. Removal of promoter nucleosomes by disassembly rather than sliding in vivo. Molecular Cell, 14(5): 667-673.
  • 11. Bonini, B.M., Van Dijck, P. & Thevelein, J.M. 2003. Uncoupling of the glucose growth defect and the deregulation of glycolysis in Saccharomyces cerevisiae Tps1 mutants expressing trehalose-6-phosphate-insensitive hexokinase from Schizosaccharomyces pombe. Biochim Biophys Acta, 1606: 83-93.
  • 12. Brachmann, C.B., Davies, A., Cost, G.J., Caputo, E., Li, J., Hieter, P. & Boeke, J.D. 1998. Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast, 14(2): 115-132.
  • 13. Chen, Y.C. & Dent, S.Y.R. 2021. Conservation and diversity of the eukaryotic SAGA coactivator complex across kingdoms. Epigenetics & Chromatin, 14 (26): 1-11.
  • 14. Chen, Y. & Futcher, B. 2017. Assaying Glycogen and Trehalose in Yeast. Bio-Protocol, 7(13): e2371.
  • 15. Deroover, S., Ghillebert, R., Broeckx, T., Winderickx, J. & Rolland, F. 2016. Trehalose-6-phosphate synthesis controls yeast gluconeogenesis downstream and independent of SNF1. FEMS Yeast Research, 16(4): 1-15.
  • 16. Eleutherio, E., Panek, A., De Mesquita, J.F., Trevisol, E. & Magalhães, R. 2015. Revisiting yeast trehalose metabolism. Current Genetics, 61: 263-274.
  • 17. Engel, S.R., Dietrich, F.S., Fisk, D.G., Binkley, G., Balakrishnan, R., Costanzo, M.C., Dwight, S.S., Hitz, B.C., Karra, K., Nash, R.S., Weng, S., Wong, E.D., Lloyd, P., Skrzypek, M.S., Miyasato, S.R., Simison, M. & Cherry, J.M. 2014. The reference genome sequence of Saccharomyces cerevisiae: Then and now. G3:Genes-Genomes-Genetics, 4(3): 389-398. http://sgd-archive.yeastgenome.org (Date accessed: 19.10.2021)
  • 18. Estruch, F. 2000. Stress-controlled transcription factors, stress-induced genes and stress tolerance in budding yeast. FEMS Microbiology Reviews, 24(4): 469-486.
  • 19. Fazzio, T.G. & Tsukiyama, T. 2003. Chromatin remodeling in vivo: Evidence for a nucleosome sliding mechanism. Molecular Cell, 12(5): 1333-1340.
  • 20. Flores, C.L., Gancedo, C. & Petit, T. 2011. Disruption of Yarrowia lipolytica TPS1 gene encoding trehalose-6-P synthase does not affect growth in glucose but impairs growth at high temperature. PLoS One, 6(9): e23695.
  • 21. François, J. & Parrou, J.L. 2001. Reserve carbohydrates metabolism in the yeast Saccharomyces cerevisiae. FEMS Microbiol Reviews, 25(1): 125-145.
  • 22. Gancedo, C., Flores, C.L. & Gancedo, J.M. 2016. The expanding landscape of moonlighting proteins in yeasts. Microbiology and Molecular Biology Reviews, 80(3): 765-77.
  • 23. Garre, E., Pérez‐Torrado, R., Gimeno‐Alcañiz, J.V. & Matallana, E. 2009. Acid trehalase is involved in intracellular trehalose mobilization during post-diauxic growth and severe saline stress in Saccharomyces cerevisiae. FEMS Yeast Research, 9(1): 52-62.
  • 24. Gasch, A.P., Spellman, P.T., Kao, C.M., Carmel-Harel, O., Eisen, M.B., Storz, G., Botstein, D. & Brown, P.O. 2000. Genomic expression programs in the response of yeast cells to environmental changes. Molecular Biology of the Cell, 11(12): 4241-4257.
  • 25. Gibney, P.A., Schieler, A., Chen, J.C., Rabinowitz, J.D. & Botstein, D. 2015. Characterizing the in vivo role of trehalose in Saccharomyces cerevisiae using the AGT1 transporter. Proceedings of the National Academy of Sciences, 112(19): 6116-6121.
  • 26. Görner, W., Durchschlag, E., Wolf, J., Brown, E.L., Ammerer, G., Ruis, H. & Schüller, C. 2002. Acute glucose starvation activates the nuclear localization signal of a stress-specific yeast transcription factor. EMBO Journal, 21(1-2): 135-144.
  • 27. Guarente, L. 1983. Yeast promoters and lacZ fusions designed to study expression of cloned genes in yeast. Methods in Enzymology, 101: 181-191.
  • 28. Huebert, D.J., Kuan, P., Keleş, S. & Gasch, A.P. 2012. Dynamic changes in nucleosome occupancy are not predictive of gene expression dynamics but are linked to transcription and chromatin regulators. Molecular and Cellular Biology, 32(9): 1645-1653.
  • 29. Jules, M., Beltran, G., François, J. & Parrou, J.L. 2008. New insights into trehalose metabolism by Saccharomyces cerevisiae: NTH2 encodes a functional cytosolic trehalase, and deletion of TPS1 reveals Ath1p-dependent trehalose mobilization. Applied and Environmental Microbiology, 74(3): 605-614.
  • 30. Jules, M., Guillou, V., François, J. & Parrou, J.L. 2004. Two distinct pathways for trehalose assimilation in the yeast Saccharomyces cerevisiae. Applied and Environmental Microbiology, 70(5): 2771-2778.
  • 31. Kocaefe-Özşen, N., Yilmaz, B., Alkım, C., Arslan, M., Topaloğlu, A., Kısakesen, H.L.B., Gülsev E., Çakar Z.P. 2022. Physiological and molecular characterization of an oxidative stress-resistant Saccharomyces cerevisiae strain obtained by evolutionary engineering. Frontiers in Microbiology, 13: 822864.
  • 32. Lee, T.I., Causton, H.C., Holstege, F.C., Shen, W.C., Hannett, N., Jennings, E.G., Winston, F., Green, M.R. & Young, R.A. 2000. Redundant roles for the TFIID and SAGA complexes in global transcription. Nature, 405: 701-704.
  • 33. Lillie, S.H. & Pringle, J.R. 1980. Reserve carbohydrate metabolism in Saccharomyces cerevisiae: responses to nutrient limitation. Journal of Bacteriology, 143: 1384-1394.
  • 34. Lowry, O.H., Rosebrough N.J. & Farr A.L. 1951. Randall RJ. Protein measurement with the folin Phenol reagent. Journal of Biological Chemistry, 193(1): 265-275.
  • 35. Magalhães, R.S.S., Popova, B., Braus, G.H., Outeiro, T.F. & Eleutherio, E.C.A. 2018. The trehalose protective mechanism during thermal stress in Saccharomyces cerevisiae: the roles of Ath1 and Agt1. FEMS Yeast Research, 18(6): 1-10.
  • 36. Martinez-Pastor, M.T., Marchler, G., Schüller, C., Marchler-Bauer, A., Ruis, H. & Estruch, F. 1996. The Saccharomyces cerevisiae zinc finger proteins Msn2p and Msn4p are required for transcriptional induction through the stress response element (STRE). EMBO Journal, 15(9): 2227-2235.
  • 37. Meylan, P., Dreos, R., Ambrosini, G., Groux, R. & Bucher, P. 2020. EPD in 2020: enhanced data visualization and extension to ncRNA promoters. Nucleic Acids Research, 48(1): 65-69. https://epd.epfl.ch//index.php (Date accessed: 19.10.2021)
  • 38. Monteiro, P.T., Oliveira, J., Pais, P., Antunes, M., Palma, M., Cavalheiro, M., Galocha, M., Godinho, C.P., Martins, L.C., Bourbon, N, Mota, M.N., Ribeiro, R.A., Viana, R., Sá-Correia, I. & Teixeira, M.C. 2020. YEASTRACT+: a portal for cross-species comparative genomics of transcription regulation in yeasts. Nucleic Acids Research, 48(1): 642-649. http://www.yeastract.com (Date accessed: 19.10.2021)
  • 39. Nagy, Z. & Tora, L. 2007. Distinct GCN5/PCAF-containing complexes function as co-activators and are involved in transcription factor and global histone acetylation. Oncogene, 26(37): 5341-5357.
  • 40. Narlikar, G.J., Fan, H.Y. & Kingston, R.E. 2002. Cooperation between complexes that regulate chromatin structure and transcription. Cell, 108(4): 475-487.
  • 41. Nwaka, S. & Holzer, H. 1997. Molecular biology of trehalose and the trehalases in the yeast Saccharomyces cerevisiae. Progress in Nucleic Acid Research and Molecular Biology, 58: 197-237.
  • 42. Nwaka, S., Kopp, M. & Holzer, H. 1995. Expression and function of the trehalase genes NTH1 and YBR0106 in Saccharomyces cerevisiae. Journal of Biological Chemistry, 270(17): 10193-10198.
  • 43. Park, H.D., Beeser, A.E., Clancy, M.J. & Cooper, T.G. 1996. The Saccharomyces cerevisiae nitrogen starvation-induced Yvh1p and Ptp2p phosphatases play a role in control of sporulation. Yeast, 12(11): 1135-1151.
  • 44. Parrou, J.L., Enjalbert, B., Plourde, L., Bauche, A., Gonzalez, B. & François, J. 1999. Dynamic responses of reserve carbohydrate metabolism under carbon and nitrogen limitations in Saccharomyces cerevisiae. Yeast, 15(3): 191-203.
  • 45. Parrou, J.L., Teste, M.A. & François, J. 1997. Effects of various types of stress on the metabolism of reserve carbohydrates in Saccharomyces cerevisiae: Genetic evidence for a stress-induced recycling of glycogen and trehalose. Microbiology, 143(6): 1891-1900.
  • 46. Peeters, K., Van Leemputte, F., Fischer, B., Bonini, B.M., Quezada, H., Tsytlonok, M., Haesen, D., Vanthienen, W., Bernardes, N., Gonzalez-Blas, C.B., Janssens, V., Tompa, P., Versees, W. & Thevelein, J.M. 2017. Fructose-1,6-bisphosphate couples glycolytic flux to activation of Ras. Nature Communications, 8(922): 1-15.
  • 47. Rajvanshi, P.K., Arya, M. & Raiasekharan, R. 2017. The stress-regulatory transcription factors Msn2 and Msn4 regulate fatty acid oxidation in budding yeast. Journal of Biological Chemistry, 292(45): 18628-18643.
  • 48. Ricci, A.R., Genereaux, J. & Brandl, C.J. 2002. Components of the SAGA histone acetyltransferase complex are required for repressed transcription of ARG1 in rich medium. Molecular and Cellular Biology, 22(12): 4033-4042.
  • 49. Rodriguez-Navarro, S. 2009. Insights into SAGA function during gene expression. EMBO Reports, 10(8): 843-850.
  • 50. Schepers, W., Van Zeebroeck, G., Pinkse, M., Verhaert, P. & Thevelein, J.M. 2012. In vivo phosphorylation of Ser21 and Ser83 during nutrient-induced activation of the yeast protein kinase A (PKA) target trehalase. Journal of Biological Chemistry, 287(53): 44130-44142.
  • 51. Sterner, D.E., Grant, P.A., Roberts, S.M., Duggan, L.J., Belotserkovskaya, R., Pacella, L.A., Winston, F., Workman, J.L. & Berger, S.L. 1999. Functional organization of the yeast SAGA complex: Distinct components involved in structural integrity, nucleosome acetylation, and TATA-binding protein interaction. Molecular and Cellular Biology, 19(1): 86-98.
  • 52. Stewart-Ornstein, J., Nelson, C., De Risi, J., Weissman, J.S. & El-Samad, H. 2013. Msn2 coordinates a stoichiometric gene expression program. Current Biology, 23(23): 2336-2345.
  • 53. Stolz, R.C. & Bishop, T.C. 2010. ICM web: the interactive chromatin modeling web server. Nucleic Acids Research, 38(2): 254-261. http://dna.engr.latech.edu/icm-du/index.php (Date accessed: 14.11.2021)
  • 54. Sürmeli, Y., Holyavkin, C., Topaloğlu, A., Arslan, M., Kısakesen, H.İ. & Çakar, Z.P. 2019. Evolutionary engineering and molecular characterization of a caffeine-resistant Saccharomyces cerevisiae strain. World Journal of Microbiology and Biotechnology, 35: 183.
  • 55. Thevelein, J.M. 1984. Regulation of trehalose mobilization in fungi. Microbiological Reviews, 48: 42-59.
  • 56. Trevisol, E.T.V., Panek, A.D., De Mesquita, J.F. & Eleutherio, E.C.A. 2014. Regulation of the yeast trehalose-synthase complex by cyclic AMP-dependent phosphorylation. Biochimica et Biophysica Acta, 1840(6): 1646-1650.
  • 57. Türkel, S., Turgut, T., Lopez, M.C., Uemura, H. & Baker, H.V. 2003a. Mutations in GCR1 affect SUC2 gene expression in Saccharomyces cerevisiae. Molecular Genetics and Genomics, 268(6): 825-831.
  • 58. Türkel, S., Turgut, T. & Savaşçıoğlu, İ. 2003b. Analysis of the effects of transcription factors Gcr2p and Sgc1p on the control of the SUC2 gene expression in Saccharomyces cerevisiae. Turkish Journal of Biology, 27: 233-239.
  • 59. Winderickx, J., De Winde, J.H., Crauwels, M., Hino, A., Hohman, S., Van Dijck, P. & Thevelein, J.M. 1996. Regulation of genes encoding subunits of the trehalose synthase complex in Saccharomyces cerevisiae: Novel variations of STRE-mediated transcription control? Molecular and General Genetics, 252(4): 470-482.
  • 60. Wu, P.Y.J. & Winston, F. 2002. Analysis of Spt7 function in the Saccharomyces cerevisiae SAGA coactivator complex. Molecular and Cellular Biology, 22(15): 5367-5379.
  • 61. Yo, K.O., Jung, J., Ramzi, A.B., Choe, S.H., Kim, S.W., Park, C. & Han, S.O. 2012. Increased ethanol production from glycerol by Saccharomyces cerevisiae strains with enhanced stress tolerance from the overexpression of SAGA complex components. Enzyme and Microbial Technology, 51(4): 237-243.
  • 62. Yu, R., Cao, X., Sun, L., Zhu, J., Wasko, B.M., Liu, W., Crutcher, E., Liu, H., Jo, M.C., Qin, L., Kaeberlein, M., Han, Z. & Dang, W. 2021. Inactivating histone deacetylase HDA promotes longevity by mobilizing trehalose metabolism. Nature Communications, 12: 1-16.
  • 63. Zähringer, H., Burgert, M., Holzer, H. & Nwaka, S. 1997. Neutral trehalase Nth1p of Saccharomyces cerevisiae encoded by the NTH1 gene is a multiple stress responsive protein. FEBS Letters, 412(3): 615-620.
  • 64. Zähringer, H., Thevelein, J.M. & Nwaka, S. 2000. Induction of neutral trehalase Nth1 by heat and osmotic stress is controlled by STRE elements and Msn2/Msn4 transcription factors: Variations of PKA effect during stress and growth. Molecular Microbiology, 35(2): 397-406.
  • 65. Zaim, J., Speina, E. & Kierzek, A.M. 2005. Identification of new genes regulated by the Crt1 transcription factor, an effector of the DNA damage checkpoint pathway in Saccharomyces cerevisiae. Journal of Biological Chemistry, 280(1): 28-37.

Year 2022, , 167 - 176, 15.10.2022

Tulay Turgut Genc

https://doi.org/10.23902/trkjnat.1131400
Cited By: 1

Abstract

Saccharomyces cerevisiae olumsuz çevre koşullarında stres metaboliti olarak trehaloz biriktirir. Hücre içi trehaloz miktarının düzenlenmesinde trehalozun sentezi ve yıkımı önemlidir. Bu nedenle, TPS1 ve NTH1 gen ekspresyonları transkripsiyon ve translasyon sırasında sıkı bir şekilde düzenlenmektedir. Her iki genin promotor bölgesinde Stres Tepki Elementleri (STRE) bulunduğundan stres koşullarında birlikte aktive olurlar. Ancak her iki genin promotor bölgesinde benzer düzenleyici elemanların bulunması bu genlerin transkripsiyon seviyesinde farklı bir regülasyona uğradıklarını göstermektedir. Çalışmamızda, TPS1 ve NTH1 genlerinin transkripsiyonel düzenlenmesinde Spt-Ada-Gcn5 Asetiltransferaz (SAGA) kompleksinin rolü besin yönünden zayıf ortamda belirlendi. Bu amaçla, SAGA kompleksinin alt ünitesi olan Ada1p içeren yaban tip ve içermeyen Δada1 mutant maya hücreleri azot açlığında ve normal büyüme koşullarında üretildi. Ayrıca yaban tip ve mutant maya hücrelerinde trehaloz seviyesi enzimatik olarak tespit edildi. TPS1 ve NTH1 genlerinin in silico promotor analizi sonucunda Msn2/4 transkripsiyon faktörlerinin bağlanması için gerekli olan STRE dizilerinin NTH1 promotorunda nükleozomlar tarafından kapatıldığı TPS1 promotorunda ise açıkta kaldıkları belirlendi. Ada1 proteininin yokluğunda, TPS1 geninde stres kaynaklı promotor aktivasyonu gözlenirken, NTH1 geninde promotor aktivasyonu gözlenmedi. Bu sonuçlara göre, Ada1 proteininin yokluğunda STRE dizilerini kaplayan nükleozomlar mobilize edilemediğinden Msn2/4 transkripsiyon faktörleri stres koşullarında promotora bağlanamayarak transkripsiyonu aktive edememiş olabilir. Ayrıca stres koşullarından bağımsız olarak Ada1 proteininin yokluğunda maya hücrelerindeki trehaloz birikiminin azaldığı gözlendi.

References

  • 1. Antonazzi, F., Di Felice, F. & Camilloni, G. 2021. GCN5 enables HSP12 induction promoting chromatin remodeling, not histone acetylation. Biochemistry and Cell Biology, 99(6): 700-706.
  • 2. App, H. & Holzer, H. 1989. Purification and characterization of neutral trehalase from the yeast ABYS1 mutant. Journal of Biological Chemistry, 264(29): 17583-17588.
  • 3. Arslan, M., Holyavkin, C., Kısakesen, H.İ., Topaloğlu, H.İ., Sürmeli, Y. & Çakar, Z.P. 2018. Physiological and transcriptomic analysis of a chronologically long-lived Saccharomyces cerevisiae strain obtained by evolutionary engineering. Molecular Biotechnology, 60: 468-484.
  • 4. Asada, R., Watanabe, T., Tanaka, Y., Kishida, M. & Furuta, M. 2022. Trehalose accumulation and radiation resistance due to prior heat stress in Saccharomyces cerevisiae. Archives of Microbiology, 204(5): 275.
  • 5. Ausubel, S.M., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A. & Struhl, K. 1993. Basic techniques of yeast genetics, pp 13.7.1-13.7.2. In: Ausubel, S.M., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A. & Struhl, K. (eds). Current Protocols in Molecular Biology, John Wiley & Sons, Inc., New York, 29B.3.22 pp.
  • 6. Balaban, B.G., Yılmaz, Ü., Alkım, C., Topaloğlu, A., Kısakesen, H.İ., Holyavkin, C. & Çakar, Z.P. 2019. Evolutionary engineering of an iron-resistant Saccharomyces cerevisiae mutant and its physiological and molecular characterization. Microorganisms, 8(1): 43.
  • 7. Beck, T. & Hall, M.N. 1999. The TOR signalling pathway controls nuclear localization of nutrient-regulated transcription factors. Nature, 402: 689-692.
  • 8. Bell, W., Sun, W., Hohmann, S., Wera, S., Reinders, A., De Virgilio, C. & Wiemken, A. 1998. Composition and functional analysis of the Saccharomyces cerevisiae trehalose synthase complex. Journal of Biological Chemistry, 273(50): 33311-33319.
  • 9. Belotserkovskaya, R., Sterner, D.E., Deng, M., Sayre, M.H., Lieberman, P.M. & Berger, S.L. 2000. Inhibition of TATA-binding protein function by SAGA subunits Spt3 and Spt8 at Gcn4-activated promoters. Molecular and Cellular Biology, 20(2): 634-647.
  • 10. Boeger, H., Griesenbeck, J., Strattan, J.S. & Kornberg, R.D. 2004. Removal of promoter nucleosomes by disassembly rather than sliding in vivo. Molecular Cell, 14(5): 667-673.
  • 11. Bonini, B.M., Van Dijck, P. & Thevelein, J.M. 2003. Uncoupling of the glucose growth defect and the deregulation of glycolysis in Saccharomyces cerevisiae Tps1 mutants expressing trehalose-6-phosphate-insensitive hexokinase from Schizosaccharomyces pombe. Biochim Biophys Acta, 1606: 83-93.
  • 12. Brachmann, C.B., Davies, A., Cost, G.J., Caputo, E., Li, J., Hieter, P. & Boeke, J.D. 1998. Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast, 14(2): 115-132.
  • 13. Chen, Y.C. & Dent, S.Y.R. 2021. Conservation and diversity of the eukaryotic SAGA coactivator complex across kingdoms. Epigenetics & Chromatin, 14 (26): 1-11.
  • 14. Chen, Y. & Futcher, B. 2017. Assaying Glycogen and Trehalose in Yeast. Bio-Protocol, 7(13): e2371.
  • 15. Deroover, S., Ghillebert, R., Broeckx, T., Winderickx, J. & Rolland, F. 2016. Trehalose-6-phosphate synthesis controls yeast gluconeogenesis downstream and independent of SNF1. FEMS Yeast Research, 16(4): 1-15.
  • 16. Eleutherio, E., Panek, A., De Mesquita, J.F., Trevisol, E. & Magalhães, R. 2015. Revisiting yeast trehalose metabolism. Current Genetics, 61: 263-274.
  • 17. Engel, S.R., Dietrich, F.S., Fisk, D.G., Binkley, G., Balakrishnan, R., Costanzo, M.C., Dwight, S.S., Hitz, B.C., Karra, K., Nash, R.S., Weng, S., Wong, E.D., Lloyd, P., Skrzypek, M.S., Miyasato, S.R., Simison, M. & Cherry, J.M. 2014. The reference genome sequence of Saccharomyces cerevisiae: Then and now. G3:Genes-Genomes-Genetics, 4(3): 389-398. http://sgd-archive.yeastgenome.org (Date accessed: 19.10.2021)
  • 18. Estruch, F. 2000. Stress-controlled transcription factors, stress-induced genes and stress tolerance in budding yeast. FEMS Microbiology Reviews, 24(4): 469-486.
  • 19. Fazzio, T.G. & Tsukiyama, T. 2003. Chromatin remodeling in vivo: Evidence for a nucleosome sliding mechanism. Molecular Cell, 12(5): 1333-1340.
  • 20. Flores, C.L., Gancedo, C. & Petit, T. 2011. Disruption of Yarrowia lipolytica TPS1 gene encoding trehalose-6-P synthase does not affect growth in glucose but impairs growth at high temperature. PLoS One, 6(9): e23695.
  • 21. François, J. & Parrou, J.L. 2001. Reserve carbohydrates metabolism in the yeast Saccharomyces cerevisiae. FEMS Microbiol Reviews, 25(1): 125-145.
  • 22. Gancedo, C., Flores, C.L. & Gancedo, J.M. 2016. The expanding landscape of moonlighting proteins in yeasts. Microbiology and Molecular Biology Reviews, 80(3): 765-77.
  • 23. Garre, E., Pérez‐Torrado, R., Gimeno‐Alcañiz, J.V. & Matallana, E. 2009. Acid trehalase is involved in intracellular trehalose mobilization during post-diauxic growth and severe saline stress in Saccharomyces cerevisiae. FEMS Yeast Research, 9(1): 52-62.
  • 24. Gasch, A.P., Spellman, P.T., Kao, C.M., Carmel-Harel, O., Eisen, M.B., Storz, G., Botstein, D. & Brown, P.O. 2000. Genomic expression programs in the response of yeast cells to environmental changes. Molecular Biology of the Cell, 11(12): 4241-4257.
  • 25. Gibney, P.A., Schieler, A., Chen, J.C., Rabinowitz, J.D. & Botstein, D. 2015. Characterizing the in vivo role of trehalose in Saccharomyces cerevisiae using the AGT1 transporter. Proceedings of the National Academy of Sciences, 112(19): 6116-6121.
  • 26. Görner, W., Durchschlag, E., Wolf, J., Brown, E.L., Ammerer, G., Ruis, H. & Schüller, C. 2002. Acute glucose starvation activates the nuclear localization signal of a stress-specific yeast transcription factor. EMBO Journal, 21(1-2): 135-144.
  • 27. Guarente, L. 1983. Yeast promoters and lacZ fusions designed to study expression of cloned genes in yeast. Methods in Enzymology, 101: 181-191.
  • 28. Huebert, D.J., Kuan, P., Keleş, S. & Gasch, A.P. 2012. Dynamic changes in nucleosome occupancy are not predictive of gene expression dynamics but are linked to transcription and chromatin regulators. Molecular and Cellular Biology, 32(9): 1645-1653.
  • 29. Jules, M., Beltran, G., François, J. & Parrou, J.L. 2008. New insights into trehalose metabolism by Saccharomyces cerevisiae: NTH2 encodes a functional cytosolic trehalase, and deletion of TPS1 reveals Ath1p-dependent trehalose mobilization. Applied and Environmental Microbiology, 74(3): 605-614.
  • 30. Jules, M., Guillou, V., François, J. & Parrou, J.L. 2004. Two distinct pathways for trehalose assimilation in the yeast Saccharomyces cerevisiae. Applied and Environmental Microbiology, 70(5): 2771-2778.
  • 31. Kocaefe-Özşen, N., Yilmaz, B., Alkım, C., Arslan, M., Topaloğlu, A., Kısakesen, H.L.B., Gülsev E., Çakar Z.P. 2022. Physiological and molecular characterization of an oxidative stress-resistant Saccharomyces cerevisiae strain obtained by evolutionary engineering. Frontiers in Microbiology, 13: 822864.
  • 32. Lee, T.I., Causton, H.C., Holstege, F.C., Shen, W.C., Hannett, N., Jennings, E.G., Winston, F., Green, M.R. & Young, R.A. 2000. Redundant roles for the TFIID and SAGA complexes in global transcription. Nature, 405: 701-704.
  • 33. Lillie, S.H. & Pringle, J.R. 1980. Reserve carbohydrate metabolism in Saccharomyces cerevisiae: responses to nutrient limitation. Journal of Bacteriology, 143: 1384-1394.
  • 34. Lowry, O.H., Rosebrough N.J. & Farr A.L. 1951. Randall RJ. Protein measurement with the folin Phenol reagent. Journal of Biological Chemistry, 193(1): 265-275.
  • 35. Magalhães, R.S.S., Popova, B., Braus, G.H., Outeiro, T.F. & Eleutherio, E.C.A. 2018. The trehalose protective mechanism during thermal stress in Saccharomyces cerevisiae: the roles of Ath1 and Agt1. FEMS Yeast Research, 18(6): 1-10.
  • 36. Martinez-Pastor, M.T., Marchler, G., Schüller, C., Marchler-Bauer, A., Ruis, H. & Estruch, F. 1996. The Saccharomyces cerevisiae zinc finger proteins Msn2p and Msn4p are required for transcriptional induction through the stress response element (STRE). EMBO Journal, 15(9): 2227-2235.
  • 37. Meylan, P., Dreos, R., Ambrosini, G., Groux, R. & Bucher, P. 2020. EPD in 2020: enhanced data visualization and extension to ncRNA promoters. Nucleic Acids Research, 48(1): 65-69. https://epd.epfl.ch//index.php (Date accessed: 19.10.2021)
  • 38. Monteiro, P.T., Oliveira, J., Pais, P., Antunes, M., Palma, M., Cavalheiro, M., Galocha, M., Godinho, C.P., Martins, L.C., Bourbon, N, Mota, M.N., Ribeiro, R.A., Viana, R., Sá-Correia, I. & Teixeira, M.C. 2020. YEASTRACT+: a portal for cross-species comparative genomics of transcription regulation in yeasts. Nucleic Acids Research, 48(1): 642-649. http://www.yeastract.com (Date accessed: 19.10.2021)
  • 39. Nagy, Z. & Tora, L. 2007. Distinct GCN5/PCAF-containing complexes function as co-activators and are involved in transcription factor and global histone acetylation. Oncogene, 26(37): 5341-5357.
  • 40. Narlikar, G.J., Fan, H.Y. & Kingston, R.E. 2002. Cooperation between complexes that regulate chromatin structure and transcription. Cell, 108(4): 475-487.
  • 41. Nwaka, S. & Holzer, H. 1997. Molecular biology of trehalose and the trehalases in the yeast Saccharomyces cerevisiae. Progress in Nucleic Acid Research and Molecular Biology, 58: 197-237.
  • 42. Nwaka, S., Kopp, M. & Holzer, H. 1995. Expression and function of the trehalase genes NTH1 and YBR0106 in Saccharomyces cerevisiae. Journal of Biological Chemistry, 270(17): 10193-10198.
  • 43. Park, H.D., Beeser, A.E., Clancy, M.J. & Cooper, T.G. 1996. The Saccharomyces cerevisiae nitrogen starvation-induced Yvh1p and Ptp2p phosphatases play a role in control of sporulation. Yeast, 12(11): 1135-1151.
  • 44. Parrou, J.L., Enjalbert, B., Plourde, L., Bauche, A., Gonzalez, B. & François, J. 1999. Dynamic responses of reserve carbohydrate metabolism under carbon and nitrogen limitations in Saccharomyces cerevisiae. Yeast, 15(3): 191-203.
  • 45. Parrou, J.L., Teste, M.A. & François, J. 1997. Effects of various types of stress on the metabolism of reserve carbohydrates in Saccharomyces cerevisiae: Genetic evidence for a stress-induced recycling of glycogen and trehalose. Microbiology, 143(6): 1891-1900.
  • 46. Peeters, K., Van Leemputte, F., Fischer, B., Bonini, B.M., Quezada, H., Tsytlonok, M., Haesen, D., Vanthienen, W., Bernardes, N., Gonzalez-Blas, C.B., Janssens, V., Tompa, P., Versees, W. & Thevelein, J.M. 2017. Fructose-1,6-bisphosphate couples glycolytic flux to activation of Ras. Nature Communications, 8(922): 1-15.
  • 47. Rajvanshi, P.K., Arya, M. & Raiasekharan, R. 2017. The stress-regulatory transcription factors Msn2 and Msn4 regulate fatty acid oxidation in budding yeast. Journal of Biological Chemistry, 292(45): 18628-18643.
  • 48. Ricci, A.R., Genereaux, J. & Brandl, C.J. 2002. Components of the SAGA histone acetyltransferase complex are required for repressed transcription of ARG1 in rich medium. Molecular and Cellular Biology, 22(12): 4033-4042.
  • 49. Rodriguez-Navarro, S. 2009. Insights into SAGA function during gene expression. EMBO Reports, 10(8): 843-850.
  • 50. Schepers, W., Van Zeebroeck, G., Pinkse, M., Verhaert, P. & Thevelein, J.M. 2012. In vivo phosphorylation of Ser21 and Ser83 during nutrient-induced activation of the yeast protein kinase A (PKA) target trehalase. Journal of Biological Chemistry, 287(53): 44130-44142.
  • 51. Sterner, D.E., Grant, P.A., Roberts, S.M., Duggan, L.J., Belotserkovskaya, R., Pacella, L.A., Winston, F., Workman, J.L. & Berger, S.L. 1999. Functional organization of the yeast SAGA complex: Distinct components involved in structural integrity, nucleosome acetylation, and TATA-binding protein interaction. Molecular and Cellular Biology, 19(1): 86-98.
  • 52. Stewart-Ornstein, J., Nelson, C., De Risi, J., Weissman, J.S. & El-Samad, H. 2013. Msn2 coordinates a stoichiometric gene expression program. Current Biology, 23(23): 2336-2345.
  • 53. Stolz, R.C. & Bishop, T.C. 2010. ICM web: the interactive chromatin modeling web server. Nucleic Acids Research, 38(2): 254-261. http://dna.engr.latech.edu/icm-du/index.php (Date accessed: 14.11.2021)
  • 54. Sürmeli, Y., Holyavkin, C., Topaloğlu, A., Arslan, M., Kısakesen, H.İ. & Çakar, Z.P. 2019. Evolutionary engineering and molecular characterization of a caffeine-resistant Saccharomyces cerevisiae strain. World Journal of Microbiology and Biotechnology, 35: 183.
  • 55. Thevelein, J.M. 1984. Regulation of trehalose mobilization in fungi. Microbiological Reviews, 48: 42-59.
  • 56. Trevisol, E.T.V., Panek, A.D., De Mesquita, J.F. & Eleutherio, E.C.A. 2014. Regulation of the yeast trehalose-synthase complex by cyclic AMP-dependent phosphorylation. Biochimica et Biophysica Acta, 1840(6): 1646-1650.
  • 57. Türkel, S., Turgut, T., Lopez, M.C., Uemura, H. & Baker, H.V. 2003a. Mutations in GCR1 affect SUC2 gene expression in Saccharomyces cerevisiae. Molecular Genetics and Genomics, 268(6): 825-831.
  • 58. Türkel, S., Turgut, T. & Savaşçıoğlu, İ. 2003b. Analysis of the effects of transcription factors Gcr2p and Sgc1p on the control of the SUC2 gene expression in Saccharomyces cerevisiae. Turkish Journal of Biology, 27: 233-239.
  • 59. Winderickx, J., De Winde, J.H., Crauwels, M., Hino, A., Hohman, S., Van Dijck, P. & Thevelein, J.M. 1996. Regulation of genes encoding subunits of the trehalose synthase complex in Saccharomyces cerevisiae: Novel variations of STRE-mediated transcription control? Molecular and General Genetics, 252(4): 470-482.
  • 60. Wu, P.Y.J. & Winston, F. 2002. Analysis of Spt7 function in the Saccharomyces cerevisiae SAGA coactivator complex. Molecular and Cellular Biology, 22(15): 5367-5379.
  • 61. Yo, K.O., Jung, J., Ramzi, A.B., Choe, S.H., Kim, S.W., Park, C. & Han, S.O. 2012. Increased ethanol production from glycerol by Saccharomyces cerevisiae strains with enhanced stress tolerance from the overexpression of SAGA complex components. Enzyme and Microbial Technology, 51(4): 237-243.
  • 62. Yu, R., Cao, X., Sun, L., Zhu, J., Wasko, B.M., Liu, W., Crutcher, E., Liu, H., Jo, M.C., Qin, L., Kaeberlein, M., Han, Z. & Dang, W. 2021. Inactivating histone deacetylase HDA promotes longevity by mobilizing trehalose metabolism. Nature Communications, 12: 1-16.
  • 63. Zähringer, H., Burgert, M., Holzer, H. & Nwaka, S. 1997. Neutral trehalase Nth1p of Saccharomyces cerevisiae encoded by the NTH1 gene is a multiple stress responsive protein. FEBS Letters, 412(3): 615-620.
  • 64. Zähringer, H., Thevelein, J.M. & Nwaka, S. 2000. Induction of neutral trehalase Nth1 by heat and osmotic stress is controlled by STRE elements and Msn2/Msn4 transcription factors: Variations of PKA effect during stress and growth. Molecular Microbiology, 35(2): 397-406.
  • 65. Zaim, J., Speina, E. & Kierzek, A.M. 2005. Identification of new genes regulated by the Crt1 transcription factor, an effector of the DNA damage checkpoint pathway in Saccharomyces cerevisiae. Journal of Biological Chemistry, 280(1): 28-37.
There are 65 citations in total.

Details

Primary Language English
Subjects Structural Biology
Journal Section Research Article/Araştırma Makalesi
Authors

Tulay Turgut Genc 0000-0001-5074-3572

Publication Date October 15, 2022
Submission Date June 15, 2022
Acceptance Date September 5, 2022
Published in Issue Year 2022

Cite

APA Turgut Genc, T. (2022). THE SAGA COMPLEX IS ESSENTIAL FOR THE REGULATION OF GENES INVOLVED IN YEAST TREHALOSE METABOLISM. Trakya University Journal of Natural Sciences, 23(2), 167-176. https://doi.org/10.23902/trkjnat.1131400
AMA Turgut Genc T. THE SAGA COMPLEX IS ESSENTIAL FOR THE REGULATION OF GENES INVOLVED IN YEAST TREHALOSE METABOLISM. Trakya Univ J Nat Sci. October 2022;23(2):167-176. doi:10.23902/trkjnat.1131400
Chicago Turgut Genc, Tulay. “THE SAGA COMPLEX IS ESSENTIAL FOR THE REGULATION OF GENES INVOLVED IN YEAST TREHALOSE METABOLISM”. Trakya University Journal of Natural Sciences 23, no. 2 (October 2022): 167-76. https://doi.org/10.23902/trkjnat.1131400.
EndNote Turgut Genc T (October 1, 2022) THE SAGA COMPLEX IS ESSENTIAL FOR THE REGULATION OF GENES INVOLVED IN YEAST TREHALOSE METABOLISM. Trakya University Journal of Natural Sciences 23 2 167–176.
IEEE T. Turgut Genc, “THE SAGA COMPLEX IS ESSENTIAL FOR THE REGULATION OF GENES INVOLVED IN YEAST TREHALOSE METABOLISM”, Trakya Univ J Nat Sci, vol. 23, no. 2, pp. 167–176, 2022, doi: 10.23902/trkjnat.1131400.
ISNAD Turgut Genc, Tulay. “THE SAGA COMPLEX IS ESSENTIAL FOR THE REGULATION OF GENES INVOLVED IN YEAST TREHALOSE METABOLISM”. Trakya University Journal of Natural Sciences 23/2 (October 2022), 167-176. https://doi.org/10.23902/trkjnat.1131400.
JAMA Turgut Genc T. THE SAGA COMPLEX IS ESSENTIAL FOR THE REGULATION OF GENES INVOLVED IN YEAST TREHALOSE METABOLISM. Trakya Univ J Nat Sci. 2022;23:167–176.
MLA Turgut Genc, Tulay. “THE SAGA COMPLEX IS ESSENTIAL FOR THE REGULATION OF GENES INVOLVED IN YEAST TREHALOSE METABOLISM”. Trakya University Journal of Natural Sciences, vol. 23, no. 2, 2022, pp. 167-76, doi:10.23902/trkjnat.1131400.
Vancouver Turgut Genc T. THE SAGA COMPLEX IS ESSENTIAL FOR THE REGULATION OF GENES INVOLVED IN YEAST TREHALOSE METABOLISM. Trakya Univ J Nat Sci. 2022;23(2):167-76.

Cited By

Effect of cAMP-dependent Phosphodiesterase Activity on NTH1 Gene Expression and Reserve Carbohydrate Metabolism
Türk Doğa ve Fen Dergisi
https://doi.org/10.46810/tdfd.1394491

You can reach the journal's archive between the years of 2000-2011 via https://dergipark.org.tr/en/pub/trakyafbd/archive (Trakya University Journal of Natural Sciences (=Trakya University Journal of Science)


Creative Commons Lisansı

Trakya University Journal of Natural Sciences is licensed under Creative Commons Attribution 4.0 International License.