Trichoderma reesei XYR1 activates cellulase gene expression via interaction with the Mediator subunit TrGAL11 to recruit RNA polymerase II

English version

Autoři: Fanglin Zheng ^aff001; Yanli Cao ^aff001; Renfei Yang ^aff001; Lei Wang ^aff001; Xinxing Lv ^aff001; Weixin Zhang ^aff001; Xiangfeng Meng ^aff001; Weifeng Liu ^aff001
Působiště autorů: State Key Laboratory of Microbial Technology, Microbial Technology Institute, Shandong University, Qingdao, Shandong, People’s Republic of China ^aff001
Vyšlo v časopise: Trichoderma reesei XYR1 activates cellulase gene expression via interaction with the Mediator subunit TrGAL11 to recruit RNA polymerase II. PLoS Genet 16(9): e32767. doi:10.1371/journal.pgen.1008979
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1008979

Souhrn

The ascomycete Trichoderma reesei is a highly prolific cellulase producer. While XYR1 (Xylanase regulator 1) has been firmly established to be the master activator of cellulase gene expression in T. reesei, its precise transcriptional activation mechanism remains poorly understood. In the present study, TrGAL11, a component of the Mediator tail module, was identified as a putative interacting partner of XYR1. Deletion of Trgal11 markedly impaired the induced expression of most (hemi)cellulase genes, but not that of the major β-glucosidase encoding genes. This differential involvement of TrGAL11 in the full induction of cellulase genes was reflected by the RNA polymerase II (Pol II) recruitment on their core promoters, indicating that TrGAL11 was required for the efficient transcriptional initiation of the majority of cellulase genes. In addition, we found that TrGAL11 recruitment to cellulase gene promoters largely occurred in an XYR1-dependent manner. Although xyr1 expression was significantly tuned down without TrGAL11, the binding of XYR1 to cellulase gene promoters did not entail TrGAL11. These results indicate that TrGAL11 represents a direct in vivo target of XYR1 and may play a critical role in contributing to Mediator and the following RNA Pol II recruitment to ensure the induced cellulase gene expression.

Klíčová slova:

Cellulases – DNA transcription – Gene expression – Gene regulation – Mycelium – Saccharomyces cerevisiae – Transcriptional control – Yeast

Zdroje

1. Ansari SA, Morse RH. Mechanisms of Mediator complex action in transcriptional activation. Cell Mol Life Sci: CMLS. 2013;70(15):2743–56. Epub 2013/01/31. doi: 10.1007/s00018-013-1265-9 23361037.

2. Borggrefe T, Yue X. Interactions between subunits of the Mediator complex with gene-specific transcription factors. Semin Cell Dev Biol. 2011;22(7):759–68. Epub 2011/08/16. doi: 10.1016/j.semcdb.2011.07.022 21839847.

3. Malik S, Roeder RG. The metazoan Mediator co-activator complex as an integrative hub for transcriptional regulation. Nat Rev Genet. 2010;11(11):761–72. Epub 2010/10/14. doi: 10.1038/nrg2901 20940737; PubMed Central PMCID: PMC3217725.

4. Kornberg RD. Mediator and the mechanism of transcriptional activation. Trends Biochem Sci. 2005;30(5):235–9. Epub 2005/05/18. doi: 10.1016/j.tibs.2005.03.011 15896740.

5. Harper TM, Taatjes DJ. The complex structure and function of Mediator. J Biol Chem. 2018;293(36):13778–85. Epub 2017/09/16. doi: 10.1074/jbc.R117.794438 28912271; PubMed Central PMCID: PMC6130968.

6. Asturias FJ, Jiang YW, Myers LC, Gustafsson CM, Kornberg RD. Conserved structures of mediator and RNA polymerase II holoenzyme. Science (New York, NY). 1999;283(5404):985–7. Epub 1999/02/12. doi: 10.1126/science.283.5404.985 9974391.

7. Tsai KL, Yu X, Gopalan S, Chao TC, Zhang Y, Florens L, et al. Mediator structure and rearrangements required for holoenzyme formation. Nature. 2017;544(7649):196–201. Epub 2017/02/28. doi: 10.1038/nature21393 28241144; PubMed Central PMCID: PMC6692119.

8. Nozawa K, Schneider TR, Cramer P. Core Mediator structure at 3.4 A extends model of transcription initiation complex. Nature. 2017;545(7653):248–51. Epub 2017/05/04. doi: 10.1038/nature22328 28467824.

9. Tsai KL, Tomomori-Sato C, Sato S, Conaway RC, Conaway JW, Asturias FJ. Subunit Architecture and Functional Modular Rearrangements of the Transcriptional Mediator Complex. Cell. 2014;158(2):463. Epub 2014/07/17. doi: 10.1016/j.cell.2014.06.036 28915369.

10. Taatjes DJ, Schneider-Poetsch T, Tjian R. Distinct conformational states of nuclear receptor-bound CRSP-Med complexes. Nat Struct Mol Biol. 2004;11(7):664–71. Epub 2004/06/15. doi: 10.1038/nsmb789 15195149.

11. Jeong CJ, Yang SH, Xie Y, Zhang L, Johnston SA, Kodadek T. Evidence that Gal11 protein is a target of the Gal4 activation domain in the mediator. Biochemistry. 2001;40(31):9421–7. Epub 2001/08/02. doi: 10.1021/bi010011k 11478912.

12. Zhang F, Sumibcay L, Hinnebusch AG, Swanson MJ. A triad of subunits from the Gal11/tail domain of Srb mediator is an in vivo target of transcriptional activator Gcn4p. Mol Cell Biol. 2004;24(15):6871–86. Epub 2004/07/16. doi: 10.1128/MCB.24.15.6871-6886.2004 15254252; PubMed Central PMCID: PMC444856.

13. Kim S, Gross DS. Mediator recruitment to heat shock genes requires dual Hsf1 activation domains and mediator tail subunits Med15 and Med16. J Biol Chem. 2013;288(17):12197–213. Epub 2013/03/01. doi: 10.1074/jbc.M112.449553 23447536; PubMed Central PMCID: PMC3636903.

14. Natarajan K, Jackson BM, Zhou H, Winston F, Hinnebusch AG. Transcriptional activation by Gcn4p involves independent interactions with the SWI/SNF complex and the SRB/mediator. Mol cell. 1999;4(4):657–64. Epub 1999/11/05. doi: 10.1016/s1097-2765(00)80217-8 10549298.

15. Brzovic PS, Heikaus CC, Kisselev L, Vernon R, Herbig E, Pacheco D, et al. The acidic transcription activator Gcn4 binds the mediator subunit Gal11/Med15 using a simple protein interface forming a fuzzy complex. Mol cell. 2011;44(6):942–53. Epub 2011/12/27. doi: 10.1016/j.molcel.2011.11.008 22195967; PubMed Central PMCID: PMC3246216.

16. Herbig E, Warfield L, Fish L, Fishburn J, Knutson BA, Moorefield B, et al. Mechanism of Mediator recruitment by tandem Gcn4 activation domains and three Gal11 activator-binding domains. Mol Cell Biol. 2010;30(10):2376–90. Epub 2010/03/24. doi: 10.1128/MCB.01046-09 20308326; PubMed Central PMCID: PMC2863704.

17. Lee YC, Park JM, Min S, Han SJ, Kim YJ. An activator binding module of yeast RNA polymerase II holoenzyme. Mol Cell Biol. 1999;19(4):2967–76. Epub 1999/03/19. doi: 10.1128/mcb.19.4.2967 10082564; PubMed Central PMCID: PMC84091.

18. Degrasse JA, Devos D. A functional proteomic study of the Trypanosoma brucei nuclear pore complex: an informatic strategy. Methods Mol Biol (Clifton, NJ). 2010;673:231–8. Epub 2010/09/14. doi: 10.1007/978-1-60761-842-3_15 20835803.

19. Myers LC, Gustafsson CM, Hayashibara KC, Brown PO, Kornberg RD. Mediator protein mutations that selectively abolish activated transcription. Proc Natl Acad Sci U S A. 1999;96(1):67–72. Epub 1999/01/06. doi: 10.1073/pnas.96.1.67 9874773; PubMed Central PMCID: PMC15094.

20. Thakur JK, Arthanari H, Yang F, Chau KH, Wagner G, Naar AM. Mediator subunit Gal11p/MED15 is required for fatty acid-dependent gene activation by yeast transcription factor Oaf1p. J Biol Chem. 2009;284(7):4422–8. Epub 2008/12/06. doi: 10.1074/jbc.M808263200 19056732; PubMed Central PMCID: PMC3837390.

21. Park JM, Kim HS, Han SJ, Hwang MS, Lee YC, Kim YJ. In vivo requirement of activator-specific binding targets of mediator. Mol Cell Biol. 2000;20(23):8709–19. Epub 2000/11/14. doi: 10.1128/mcb.20.23.8709-8719.2000 11073972; PubMed Central PMCID: PMC86488.

22. Ansari SA, Morse RH. Selective role of Mediator tail module in the transcription of highly regulated genes in yeast. Transcription. 2012;3(3):110–4. Epub 2012/07/10. doi: 10.4161/trns.19840 22771944; PubMed Central PMCID: PMC3616079.

23. Wang X, Sun Q, Ding Z, Ji J, Wang J, Kong X, et al. Redefining the modular organization of the core Mediator complex. Cell Res. 2014;24(7):796–808. Epub 2014/05/09. doi: 10.1038/cr.2014.64 24810298; PubMed Central PMCID: PMC4085763.

24. Anandhakumar J, Moustafa YW, Chowdhary S, Kainth AS, Gross DS. Evidence for Multiple Mediator Complexes in Yeast Independently Recruited by Activated Heat Shock Factor. Mol Cell Biol. 2016;36(14):1943–60. Epub 2016/05/18. doi: 10.1128/MCB.00005-16 27185874; PubMed Central PMCID: PMC4936062.

25. Poss ZC, Ebmeier CC, Taatjes DJ. The Mediator complex and transcription regulation. Crit Rev Biochem Mol Biol. 2013;48(6):575–608. Epub 2013/10/04. doi: 10.3109/10409238.2013.840259 24088064; PubMed Central PMCID: PMC3852498.

26. Lynd LR, Weimer PJ, van Zyl WH, Pretorius IS. Microbial cellulose utilization: fundamentals and biotechnology. Microbiol Mol Biol Rev: MMBR. 2002;66(3):506–77, table of contents. Epub 2002/09/05. doi: 10.1128/mmbr.66.3.506-577.2002 12209002; PubMed Central PMCID: PMC120791.

27. Druzhinina IS, Kubicek CP. Genetic engineering of Trichoderma reesei cellulases and their production. Microb Biotechnol. 2017;10(6):1485–99. Epub 2017/05/31. doi: 10.1111/1751-7915.12726 28557371; PubMed Central PMCID: PMC5658622.

28. Aro N, Saloheimo A, Ilmen M, Penttila M. ACEII, a novel transcriptional activator involved in regulation of cellulase and xylanase genes of Trichoderma reesei. J Biol Chem. 2001;276(26):24309–14. Epub 2001/04/17. doi: 10.1074/jbc.M003624200 11304525.

29. Hakkinen M, Valkonen MJ, Westerholm-Parvinen A, Aro N, Arvas M, Vitikainen M, et al. Screening of candidate regulators for cellulase and hemicellulase production in Trichoderma reesei and identification of a factor essential for cellulase production. Biotechnol Biofuels. 2014;7(1):14. Epub 2014/01/30. doi: 10.1186/1754-6834-7-14 24472375; PubMed Central PMCID: PMC3922861.

30. Stricker AR, Grosstessner-Hain K, Wurleitner E, Mach RL. Xyr1 (xylanase regulator 1) regulates both the hydrolytic enzyme system and D-xylose metabolism in Hypocrea jecorina. Eukaryot cell. 2006;5(12):2128–37. Epub 2006/10/24. doi: 10.1128/EC.00211-06 17056741; PubMed Central PMCID: PMC1694815.

31. Zeilinger S, Ebner A, Marosits T, Mach R, Kubicek CP. The Hypocrea jecorina HAP 2/3/5 protein complex binds to the inverted CCAAT-box (ATTGG) within the cbh2 (cellobiohydrolase II-gene) activating element. Mol Genet Genomics. 2001;266(1):56–63. Epub 2001/10/09. doi: 10.1007/s004380100518 11589578.

32. Saloheimo A, Aro N, Ilmen M, Penttila M. Isolation of the ace1 gene encoding a Cys(2)-His(2) transcription factor involved in regulation of activity of the cellulase promoter cbh1 of Trichoderma reesei. The J Biol Chem. 2000;275(8):5817–25. Epub 2000/02/22. doi: 10.1074/jbc.275.8.5817 10681571.

33. Cao Y, Zheng F, Wang L, Zhao G, Chen G, Zhang W, et al. Rce1, a novel transcriptional repressor, regulates cellulase gene expression by antagonizing the transactivator Xyr1 in Trichoderma reesei. Mol Microbiol. 2017;105(1):65–83. doi: 10.1111/mmi.13685 28378498.

34. Chen L, Zou G, Wang J, Wang J, Liu R, Jiang Y, et al. Characterization of the Ca(2+) -responsive signaling pathway in regulating the expression and secretion of cellulases in Trichoderma reesei Rut-C30. Mol Microbiol. 2016;100(3):560–75. Epub 2016/04/26. doi: 10.1111/mmi.13334 27109892.

35. Mach-Aigner AR, Pucher ME, Steiger MG, Bauer GE, Preis SJ, Mach RL. Transcriptional regulation of xyr1, encoding the main regulator of the xylanolytic and cellulolytic enzyme system in Hypocrea jecorina. Appl Environ Microbiol. 2008;74(21):6554–62. Epub 2008/09/16. doi: 10.1128/AEM.01143-08 18791032; PubMed Central PMCID: PMC2576687.

36. Seiboth B, Karimi RA, Phatale PA, Linke R, Hartl L, Sauer DG, et al. The putative protein methyltransferase LAE1 controls cellulase gene expression in Trichoderma reesei. Mol Microbiol. 2012;84(6):1150–64. Epub 2012/05/05. doi: 10.1111/j.1365-2958.2012.08083.x 22554051; PubMed Central PMCID: PMC3370264.

37. Lv X, Zheng F, Li C, Zhang W, Chen G, Liu W. Characterization of a copper responsive promoter and its mediated overexpression of the xylanase regulator 1 results in an induction-independent production of cellulases in Trichoderma reesei. Biotechnol for biofuels. 2015;8:67. Epub 2015/05/01. doi: 10.1186/s13068-015-0249-4 25926888; PubMed Central PMCID: PMC4413991.

38. Derntl C, Mach RL, Mach-Aigner AR. Fusion transcription factors for strong, constitutive expression of cellulases and xylanases in Trichoderma reesei. Biotechnol for biofuels. 2019;12:231. Epub 2019/10/05. doi: 10.1186/s13068-019-1575-8 31583017; PubMed Central PMCID: PMC6767844.

39. Lallet S, Garreau H, Garmendia-Torres C, Szestakowska D, Boy-Marcotte E, Quevillon-Cheruel S, et al. Role of Gal11, a component of the RNA polymerase II mediator in stress-induced hyperphosphorylation of Msn2 in Saccharomyces cerevisiae. Mol Microbiol. 2006;62(2):438–52. Epub 2006/10/06. doi: 10.1111/j.1365-2958.2006.05363.x 17020582.

40. Thakur JK, Arthanari H, Yang F, Pan SJ, Fan X, Breger J, et al. A nuclear receptor-like pathway regulating multidrug resistance in fungi. Nature. 2008;452(7187):604–9. Epub 2008/04/04. doi: 10.1038/nature06836 18385733.

41. Zimmermann L, Stephens A, Nam SZ, Rau D, Kubler J, Lozajic M, et al. A Completely Reimplemented MPI Bioinformatics Toolkit with a New HHpred Server at its Core. J Mol Biol. 2018;430(15):2237–43. Epub 2017/12/21. doi: 10.1016/j.jmb.2017.12.007 29258817.

42. Waterhouse A, Bertoni M, Bienert S, Studer G, Tauriello G, Gumienny R, et al. SWISS-MODEL: homology modelling of protein structures and complexes. Nucleic Acids Res. 2018;46(W1):W296–w303. Epub 2018/05/23. doi: 10.1093/nar/gky427 29788355; PubMed Central PMCID: PMC6030848.

43. Myers LC, Kornberg RD. Mediator of transcriptional regulation. Am J Hum Genet. 2000;69:729–49. Epub 2000/08/31. doi: 10.1146/annurev.biochem.69.1.729 10966474.

44. Furukawa T, Shida Y, Kitagami N, Mori K, Kato M, Kobayashi T, et al. Identification of specific binding sites for XYR1, a transcriptional activator of cellulolytic and xylanolytic genes in Trichoderma reesei. Fungal Genet Biol. 2009;46(8):564–74. Epub 2009/04/28. doi: 10.1016/j.fgb.2009.04.001 19393758.

45. Levine M, Cattoglio C, Tjian R. Looping back to leap forward: transcription enters a new era. Cell. 2014;157(1):13–25. Epub 2014/04/01. doi: 10.1016/j.cell.2014.02.009 24679523; PubMed Central PMCID: PMC4059561.

46. Allen BL, Taatjes DJ. The Mediator complex: a central integrator of transcription. Nat Rev Mol Cell Biol. 2015;16(3):155–66. Epub 2015/02/19. doi: 10.1038/nrm3951 25693131; PubMed Central PMCID: PMC4963239.

47. Hantsche M, Cramer P. Conserved RNA polymerase II initiation complex structure. Curr Opin Struct Biol. 2017;47:17–22. Epub 2017/04/25. doi: 10.1016/j.sbi.2017.03.013 28437704.

48. Robinson PJ, Trnka MJ, Pellarin R, Greenberg CH, Bushnell DA, Davis R, et al. Molecular architecture of the yeast Mediator complex. eLife. 2015;4. Epub 2015/09/25. doi: 10.7554/eLife.08719 26402457; PubMed Central PMCID: PMC4631838.

49. Béve J, Hu GZ, Myers LC, Balciunas D, Werngren O, Hultenby K, et al. The structural and functional role of Med5 in the yeast Mediator tail module. J Biol Chem. 2005;280(50):41366–72. Epub 2005/10/19. doi: 10.1074/jbc.M511181200 16230344.

50. Lipford JR, Smith GT, Chi Y, Deshaies RJ. A putative stimulatory role for activator turnover in gene expression. Nature. 2005;438(7064):113–6. doi: 10.1038/nature04098 16267558.

51. Geng F, Wenzel S, Tansey WP. Ubiquitin and proteasomes in transcription. Annu Rev Biochem. 2012;81:177–201. doi: 10.1146/annurev-biochem-052110-120012 22404630; PubMed Central PMCID: PMC3637986.

52. Wang L, Lv X, Cao Y, Zheng F, Meng X, Shen Y, et al. A novel transcriptional regulator RXE1 modulates the essential transactivator XYR1 and cellulase gene expression in Trichoderma reesei. Appl Microbiol Biotechnol. 2019. Epub 2019/04/15. doi: 10.1007/s00253-019-09739-6 30982107.

53. Zhang W, Kou Y, Xu J, Cao Y, Zhao G, Shao J, et al. Two major facilitator superfamily sugar transporters from Trichoderma reesei and their roles in induction of cellulase biosynthesis. J Biol Chem. 2013;288(46):32861–72. doi: 10.1074/jbc.M113.505826 24085297; PubMed Central PMCID: PMC3829138.

54. Zheng F, Cao Y, Wang L, Lv X, Meng X, Zhang W, et al. The mating type locus protein MAT1-2-1 of Trichoderma reesei interacts with Xyr1 and regulates cellulase gene expression in response to light. Sci Rep. 2017;7(1):17346. Epub 2017/12/13. doi: 10.1038/s41598-017-17439-2 29229981; PubMed Central PMCID: PMC5725425.

55. Zhou Q, Xu J, Kou Y, Lv X, Zhang X, Zhao G, et al. Differential involvement of beta-glucosidases from Hypocrea jecorina in rapid induction of cellulase genes by cellulose and cellobiose. Eukaryot cell. 2012;11(11):1371–81. Epub 2012/09/25. doi: 10.1128/EC.00170-12 23002106; PubMed Central PMCID: PMC3486029.

56. Cao Y, Zheng F, Zhang W, Meng X, Liu W. Trichoderma reesei XYR1 recruits SWI/SNF to facilitate cellulase gene expression. Mol Microbiol. 2019;112(4):1145–62. Epub 2019/07/17. doi: 10.1111/mmi.14352 31309604.

57. Schmoll M, Franchi L, Kubicek CP. Envoy, a PAS/LOV domain protein of Hypocrea jecorina (Anamorph Trichoderma reesei), modulates cellulase gene transcription in response to light. Eukaryot cell. 2005;4(12):1998–2007. Epub 2005/12/13. doi: 10.1128/EC.4.12.1998-2007.2005 16339718; PubMed Central PMCID: PMC1317494.

58. Xu J, Zhao G, Kou Y, Zhang W, Zhou Q, Chen G, et al. Intracellular beta-glucosidases CEL1a and CEL1b are essential for cellulase induction on lactose in Trichoderma reesei. Eukaryot cell. 2014;13(8):1001–13. Epub 2014/06/01. doi: 10.1128/EC.00100-14 24879125; PubMed Central PMCID: PMC4135799.

59. Li Y, Chen G, Liu W. Multiple metabolic signals influence GAL gene activation by modulating the interaction of Gal80p with the transcriptional activator Gal4p. Mol Microbiol. 2010;78(2):414–28. doi: 10.1111/j.1365-2958.2010.07343.x 20979343

60. Yu M, Wang J, Li W, Yuan YZ, Li CY, Qian XH, et al. Proteomic screen defines the hepatocyte nuclear factor 1alpha-binding partners and identifies HMGB1 as a new cofactor of HNF1alpha. Nucleic Acids Res. 2008;36(4):1209–19. Epub 2007/12/28. doi: 10.1093/nar/gkm1131 18160415; PubMed Central PMCID: PMC2275099.

61. Ansari SA, Morse RH. Mechanisms of Mediator complex action in transcriptional activation. Cell Mol Life Sci. 2013;70(15):2743–56. doi: 10.1007/s00018-013-1265-9 23361037

Článek Alleviating chronic ER stress by p38-Ire1-Xbp1 pathway and insulin-associated autophagy in C. elegans neurons

Článek Coordinate genomic association of transcription factors controlled by an imported quorum sensing peptide in Cryptococcus neoformans

Článek Using prior information from humans to prioritize genes and gene-associated variants for complex traits in livestock

Článek The STRIPAK signaling complex regulates dephosphorylation of GUL1, an RNA-binding protein that shuttles on endosomes

Článek PIG-1 MELK-dependent phosphorylation of nonmuscle myosin II promotes apoptosis through CES-1 Snail partitioning

Článek Trappc9 deficiency causes parent-of-origin dependent microcephaly and obesity

Článek A mega-analysis of expression quantitative trait loci in retinal tissue

Článek Genetic analysis of the modern Australian labradoodle dog breed reveals an excess of the poodle genome

Článek Imaginal disc growth factor maintains cuticle structure and controls melanization in the spot pattern formation of Bombyx mori

Článek The Arabidopsis PHD-finger protein EDM2 has multiple roles in balancing NLR immune receptor gene expression

Článek A Novel Recessive Mutation in SPEG Causes Early Onset Dilated Cardiomyopathy

Článek Excess crossovers impede faithful meiotic chromosome segregation in C. elegans