Synergistic and Dose-Controlled Regulation of Cellulase Gene Expression in

English version České info

Cellulolytic fungi have evolved into sophisticated lignocellulolytic systems to adapt to their natural habitat. This trait is important for filamentous fungi, which are the main source of cellulases utilized to degrade lignocellulose to fermentable sugars. Penicillium oxalicum, which produces lignocellulolytic enzymes with more diverse components than Trichoderma reesei, has the capacity to secrete large amounts of cellulases. Meanwhile, cellulase expression is regulated by a complex network involved in many transcription factors in this organism. To better understand how cellulase genes are systematically regulated in P. oxalicum, we employed molecular genetics to uncover the cellulolytic transcription factors on a genome-wide scale. We discovered the synergistic and tunable regulation of cellulase expression by integrating cellulolytic regulators and their target genes, which refined our understanding of transcriptional-regulatory network as a “seesaw model” in which the coordinated regulation of cellulolytic genes is established by counteracting activators and repressors.

Vyšlo v časopise: Synergistic and Dose-Controlled Regulation of Cellulase Gene Expression in. PLoS Genet 11(9): e32767. doi:10.1371/journal.pgen.1005509
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005509

Souhrn

Zdroje

1. Liu G, Zhang L, Qin Y, Zou G, Li Z, et al. (2013) Long-term strain improvements accumulate mutations in regulatory elements responsible for hyper-production of cellulolytic enzymes. Scientific reports 3: 1569–1575. doi: 10.1038/srep01569 23535838

2. Glass NL, Schmoll M, Cate JH, Coradetti S (2013) Plant cell wall deconstruction by ascomycete fungi. Annu Rev Microbiol 67: 477–498. doi: 10.1146/annurev-micro-092611-150044 23808333

3. Peterson R, Nevalainen H (2012) Trichoderma reesei RUT-C30—thirty years of strain improvement. Microbiology 158: 58–68. doi: 10.1099/mic.0.054031-0 21998163

4. van den Brink J, de Vries RP (2011) Fungal enzyme sets for plant polysaccharide degradation. Appl Microbiol Biotechnol 91: 1477–1492. doi: 10.1007/s00253-011-3473-2 21785931

5. Verbeke J, Coutinho P, Mathis H, Quenot A, Record E, et al. (2009) Transcriptional profiling of cellulase and expansin-related genes in a hypercellulolytic Trichoderma reesei. Biotechnol Lett 31: 1399–1405. doi: 10.1007/s10529-009-0030-5 19479322

6. Amore A, Giacobbe S, Faraco V (2013) Regulation of cellulase and hemicellulase gene expression in fungi. Curr Genomics 14: 230–249. doi: 10.2174/1389202911314040002 24294104

7. Ebbole DJ (1998) Carbon catabolite repression of gene expression and conidiation in Neurospora crassa. Fungal Genet Biol 25: 15–21. 9806802

8. Ilmen M, Thrane C, Penttila M (1996) The glucose repressor gene cre1 of Trichoderma: isolation and expression of a full-length and a truncated mutant form. Mol Gen Genet 251: 451–460. 8709949

9. Dowzer CE, Kelly JM (1991) Analysis of the creA gene, a regulator of carbon catabolite repression in Aspergillus nidulans. Mol Cell Biol 11: 5701–5709. 1922072

10. Mach-Aigner AR, Pucher ME, Steiger MG, Bauer GE, Preis SJ, et al. (2008) Transcriptional regulation of xyr1, encoding the main regulator of the xylanolytic and cellulolytic enzyme system in Hypocrea jecorina. Appl Environ Microbiol 74: 6554–6562. doi: 10.1128/AEM.01143-08 18791032

11. van Peij NN, Visser J, de Graaff LH (1998) Isolation and analysis of xlnR, encoding a transcriptional activator co-ordinating xylanolytic expression in Aspergillus niger. Mol Microbiol 27: 131–142. 9466262

12. Sun J, Tian C, Diamond S, Glass NL (2012) Deciphering transcriptional regulatory mechanisms associated with hemicellulose degradation in Neurospora crassa. Eukaryot Cell 11: 482–493. doi: 10.1128/EC.05327-11 22345350

13. Aro N, Ilmen M, Saloheimo A, Penttila M (2003) ACEI of Trichoderma reesei is a repressor of cellulase and xylanase expression. Appl Environ Microbiol 69: 56–65. 12513977

14. Aro N, Saloheimo A, Ilmen M, Penttila M (2001) ACEII, a novel transcriptional activator involved in regulation of cellulase and xylanase genes of Trichoderma reesei. J Biol Chem 276: 24309–24314. 11304525

15. Hakkinen M, Valkonen MJ, Westerholm-Parvinen A, Aro N, Arvas M, et al. (2014) Screening of candidate regulators for cellulase and hemicellulase production in Trichoderma reesei and identification of a factor essential for cellulase production. Biotechnol Biofuels 7: 14. doi: 10.1186/1754-6834-7-14 24472375

16. Ogawa M, Kobayashi T, Koyama Y (2012) ManR, a novel Zn(II)2Cys6 transcriptional activator, controls the beta-mannan utilization system in Aspergillus oryzae. Fungal Genet Biol 49: 987–995. doi: 10.1016/j.fgb.2012.09.006 23063954

17. Coradetti ST, Craig JP, Xiong Y, Shock T, Tian C, et al. (2012) Conserved and essential transcription factors for cellulase gene expression in ascomycete fungi. Proc Natl Acad Sci U S A doi: 10.1073/pnas.1200785109

18. Nitta M, Furukawa T, Shida Y, Mori K, Kuhara S, et al. (2012) A new Zn(II)(2)Cys(6)-type transcription factor BglR regulates beta-glucosidase expression in Trichoderma reesei. Fungal Genet Biol 49: 388–397. doi: 10.1016/j.fgb.2012.02.009 22425594

19. Wang S, Liu G, Wang J, Yu J, Huang B, et al. (2013) Enhancing cellulase production in Trichoderma reesei RUT C30 through combined manipulation of activating and repressing genes. J Ind Microbiol Biotechnol 40: 633–641. doi: 10.1007/s10295-013-1253-y 23467998

20. Coradetti ST, Xiong Y, Louise Glass N (2013) Analysis of a conserved cellulase transcriptional regulator reveals inducer-independent production of cellulolytic enzymes in Neurospora crassa. MicrobiologyOpen doi: 10.1002/mbo3.94

21. Nehlin JO, Ronne H (1990) Yeast MIG1 repressor is related to the mammalian early growth response and Wilms' tumour finger proteins. EMBO J 9: 2891–2898. 2167835

22. de Vries RP, Visser J, de Graaff LH (1999) CreA modulates the XlnR-induced expression on xylose of Aspergillus niger genes involved in xylan degradation. Res Microbiol 150: 281–285. 10376490

23. Kubicek CP, Portnoy T, Margeot A, Linke R, Atanasova L, et al. (2011) The CRE1 carbon catabolite repressor of the fungus Trichoderma reesei: a master regulator of carbon assimilation. BMC Genomics 12

24. Liu G, Zhang L, Wei X, Zou G, Qin Y, et al. (2013) Genomic and secretomic analyses reveal unique features of the lignocellulolytic enzyme system of Penicillium decumbens. PLoS One 8: e55185. doi: 10.1371/journal.pone.0055185 23383313

25. Kubicek CP, Mikus M, Schuster A, Schmoll M, Seiboth B (2009) Metabolic engineering strategies for the improvement of cellulase production by Hypocrea jecorina. Biotechnol Biofuels 2: 19. doi: 10.1186/1754-6834-2-19 19723296

26. Y Qu G L Y Q Z L (2013) Improving lignocellulolytic enzyme production with Penicillium: from strain screening to systems biology. Adv Biochem Eng Biot 4: 12.

27. Chen M, Qin Y, Cao Q, Liu G, Li J, et al. (2013) Promotion of extracellular lignocellulolytic enzymes production by restraining the intracellular beta-glucosidase in Penicillium decumbens. Bioresour Technol 137: 33–40. doi: 10.1016/j.biortech.2013.03.099 23584406

28. Zhang Y, Zhang J, Xiao P, Wang T, Qu Y (2012) Improved cellulase production via disruption of PDE01641 in cellulolytic fungus Penicillium decumbens. Bioresour Technol 123: 733–737. doi: 10.1016/j.biortech.2012.07.101 22981621

29. Li J, Liu G, Chen M, Li Z, Qin Y, et al. (2013) Cellodextrin transporters play important roles in cellulase induction in the cellulolytic fungus Penicillium oxalicum. Appl Microbiol Biotechnol doi: 10.1007/s00253-013-5301-3

30. Herpoel-Gimbert I, Margeot A, Dolla A, Jan G, Molle D, et al. (2008) Comparative secretome analyses of two Trichoderma reesei RUT-C30 and CL847 hypersecretory strains. Biotechnol Biofuels 1: 18. doi: 10.1186/1754-6834-1-18 19105830

31. Kubodera T, Yamashita N, Nishimura A (2000) Pyrithiamine resistance gene (ptrA) of Aspergillus oryzae: Cloning, characterization and application as a dominant selectable marker for transformation. Biosci Biotech Bioch 64: 1416–1421.

32. Yu JH, Hamari Z, Han KH, Seo JA, Reyes-Dominguez Y, et al. (2004) Double-joint PCR: a PCR-based molecular tool for gene manipulations in filamentous fungi. Fungal Genet Biol 41: 973–981. 15465386

33. Li ZH, Du CM, Zhong YH, Wang TH (2010) Development of a highly efficient gene targeting system allowing rapid genetic manipulations in Penicillium decumbens. Appl Microbiol Biotechnol 87: 1065–1076. doi: 10.1007/s00253-010-2566-7 20393703

34. Druzhinina IS, Seidl-Seiboth V, Herrera-Estrella A, Horwitz BA, Kenerley CM, et al. (2011) Trichoderma: the genomics of opportunistic success. Nat Rev Microbiol 9: 749–759. doi: 10.1038/nrmicro2637 21921934

35. Colot HV, Park G, Turner GE, Ringelberg C, Crew CM, et al. (2006) A high-throughput gene knockout procedure for Neurospora reveals functions for multiple transcription factors. Proc Natl Acad Sci U S A 103: 10352–10357. 16801547

36. Johnston SA, Zavortink MJ, Debouck C, Hopper JE (1986) Functional domains of the yeast regulatory protein GAL4. Proc Natl Acad Sci U S A 83: 6553–6557. 2944111

37. Punt PJ, Dingemanse MA, Jacobs-Meijsing BJ, Pouwels PH, van den Hondel CA (1988) Isolation and characterization of the glyceraldehyde-3-phosphate dehydrogenase gene of Aspergillus nidulans. Gene 69: 49–57. 3066699

38. Sun J, Glass NL (2011) Identification of the CRE-1 Cellulolytic Regulon in Neurospora crassa. PLoS One 6: e25654. doi: 10.1371/journal.pone.0025654 21980519

39. Yao G, Li Z, Gao L, Wu R, Kan Q, et al. (2015) Redesigning the regulatory pathway to enhance cellulase production in Penicillium oxalicum. Biotechnol Biofuels 8: 71. doi: 10.1186/s13068-015-0253-8 25949521

40. Lv X, Zheng F, Li C, Zhang W, Chen G, et al. (2015) 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 Biofuels 8: 67. doi: 10.1186/s13068-015-0249-4 25926888

41. Watanabe J, Tanaka H, Mogi Y, Yamazaki T, Suzuki K, et al. (2011) Loss of Aspergillus oryzae amyR function indirectly affects hemicellulolytic and cellulolytic enzyme production. J Biosci Bioeng 111: 408–413. doi: 10.1016/j.jbiosc.2010.12.006 21193346

42. Silva-Rocha R, Castro LD, Antonieto AC, Guazzaroni ME, Persinoti GF, et al. (2014) Deciphering the Cis-Regulatory Elements for XYR1 and CRE1 Regulators in Trichoderma reesei. PLoS One 9: e99366. doi: 10.1371/journal.pone.0099366 24941042

43. Ling M, Qin Y, Li N, Liang Z (2009) Binding of two transcriptional factors, Xyr1 and ACEI, in the promoter region of cellulase cbh1 gene. Biotechnol Lett 31: 227–231. doi: 10.1007/s10529-008-9857-4 18854952

44. Xiong Y, Sun J, Glass NL (2014) VIB1, a Link between Glucose Signaling and Carbon Catabolite Repression, Is Essential for Plant Cell Wall Degradation by Neurospora crassa. PLoS Genet 10: e1004500. doi: 10.1371/journal.pgen.1004500 25144221

45. Tamayo EN, Villanueva A, Hasper AA, de Graaff LH, Ramon D, et al. (2008) CreA mediates repression of the regulatory gene xlnR which controls the production of xylanolytic enzymes in Aspergillus nidulans. Fungal Genet Biol 45: 984–993. doi: 10.1016/j.fgb.2008.03.002 18420433

46. Kulmburg P, Mathieu M, Dowzer C, Kelly J, Felenbok B (1993) Specific binding sites in the alcR and alcA promoters of the ethanol regulon for the CREA repressor mediating carbon catabolite repression in Aspergillus nidulans. Mol Microbiol 7: 847–857. 8483416

47. Cziferszky A, Mach RL, Kubicek CP (2002) Phosphorylation positively regulates DNA binding of the carbon catabolite repressor Cre1 of Hypocrea jecorina (Trichoderma reesei). J Biol Chem 277: 14688–14694. 11850429

48. Martinez D, Berka RM, Henrissat B, Saloheimo M, Arvas M, et al. (2008) Genome sequencing and analysis of the biomass-degrading fungus Trichoderma reesei (syn. Hypocrea jecorina). Nat Biotechnol 26: 553–560. doi: 10.1038/nbt1403 18454138

49. Tian C, Beeson WT, Iavarone AT, Sun J, Marletta MA, et al. (2009) Systems analysis of plant cell wall degradation by the model filamentous fungus Neurospora crassa. Proc Natl Acad Sci U S A 106: 22157–22162. doi: 10.1073/pnas.0906810106 20018766

50. Zhou Q, Xu J, Kou Y, Lv X, Zhang X, et al. (2012) Differential involvement of beta-glucosidases from Hypocrea jecorina in rapid induction of cellulase genes by cellulose and cellobiose. Eukaryot Cell doi: 10.1128/EC.00170-12

51. Znameroski EA, Coradetti ST, Roche CM, Tsai JC, Iavarone AT, et al. (2012) Induction of lignocellulose-degrading enzymes in Neurospora crassa by cellodextrins. Proc Natl Acad Sci U S A 109: 6012–6017. doi: 10.1073/pnas.1118440109 22474347

52. Gruber F, Visser J, Kubicek CP, de Graaff LH (1990) The development of a heterologous transformation system for the cellulolytic fungus Trichoderma reesei based on a pyrG-negative mutant strain. Curr Genet 18: 71–76. 2245476

53. Park J, Park J, Jang S, Kim S, Kong S, et al. (2008) FTFD: an informatics pipeline supporting phylogenomic analysis of fungal transcription factors. Bioinformatics 24: 1024–1025. doi: 10.1093/bioinformatics/btn058 18304934

54. Krappmann S, Bayram O, Braus GH (2005) Deletion and allelic exchange of the Aspergillus fumigatus veA locus via a novel recyclable marker module. Eukaryot Cell 4: 1298–1307. 16002655

55. Nakayashiki H, Hanada S, Quoc NB, Kadotani N, Tosa Y, et al. (2005) RNA silencing as a tool for exploring gene function in ascomycete fungi. Fungal Genetics and Biology 42: 275–283. 15749047

56. Punt PJ, Dingemanse MA, Kuyvenhoven A, Soede RD, Pouwels PH, et al. (1990) Functional elements in the promoter region of the Aspergillus nidulans gpdA gene encoding glyceraldehyde-3-phosphate dehydrogenase. Gene 93: 101–109. 2121607

57. Sweigard J., Chumley F., Carroll A., Farrall L., V B. (1997) A series of vectors for fungal transformation. Fungal Genet Newsl 44: 52–53.

58. Penttila M, Nevalainen H, Ratto M, Salminen E, Knowles J (1987) A versatile transformation system for the cellulolytic filamentous fungus Trichoderma reesei. Gene 61: 155–164. 3127274

59. Wei X, Zheng K, Chen M, Liu G, Li J, et al. (2011) Transcription analysis of lignocellulolytic enzymes of Penicillium decumbens 114–2 and its catabolite-repression-resistant mutant. C R Biol 334: 806–811. doi: 10.1016/j.crvi.2011.06.002 22078737

60. Li R, Yu C, Li Y, Lam TW, Yiu SM, et al. (2009) SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 25: 1966–1967. doi: 10.1093/bioinformatics/btp336 19497933

61. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5: 621–628. doi: 10.1038/nmeth.1226 18516045

62. Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11: R106. doi: 10.1186/gb-2010-11-10-r106 20979621

63. Tarazona S, Garcia-Alcalde F, Dopazo J, Ferrer A, Conesa A (2011) Differential expression in RNA-seq: a matter of depth. Genome Res 21: 2213–2223. doi: 10.1101/gr.124321.111 21903743

64. Conesa A, Gotz S (2008) Blast2GO: A comprehensive suite for functional analysis in plant genomics. International journal of plant genomics 2008: 619832. doi: 10.1155/2008/619832 18483572