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

Tulay Turgut Genc

doi:10.23902/trkjnat.1131400

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

Yıl 2022, , 167 - 176, 15.10.2022

Tulay Turgut Genc

https://doi.org/10.23902/trkjnat.1131400

Cited By: 1

Öz

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.

Anahtar Kelimeler

Msn2/4, Nitrogen starvation, Nucleosome, SAGA, Trehalose

Teşekkür

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

Kaynakça

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Yıl 2022, , 167 - 176, 15.10.2022

Tulay Turgut Genc

https://doi.org/10.23902/trkjnat.1131400

Cited By: 1

Öz

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.

Kaynakça

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.
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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.
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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.
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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.
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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.
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Toplam 65 adet kaynakça vardır.

Ayrıntılar

Birincil Dil	İngilizce
Konular	Yapısal Biyoloji
Bölüm	Araştırma Makalesi/Research Article
Yazarlar	Tulay Turgut Genc 0000-0001-5074-3572
Yayımlanma Tarihi	15 Ekim 2022
Gönderilme Tarihi	15 Haziran 2022
Kabul Tarihi	5 Eylül 2022
Yayımlandığı Sayı	Yıl 2022

Kaynak Göster

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. Ekim 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, sy. 2 (Ekim 2022): 167-76. https://doi.org/10.23902/trkjnat.1131400.
EndNote	Turgut Genc T (01 Ekim 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, c. 23, sy. 2, ss. 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 (Ekim 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, c. 23, sy. 2, 2022, ss. 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.

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https://doi.org/10.46810/tdfd.1394491

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