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VIB1, a Link between Glucose Signaling and Carbon Catabolite Repression, Is Essential for Plant Cell Wall Degradation by


Many filamentous fungi that grow on plant biomass are capable of producing lignocellulase enzymes to break down plant cell walls into utilizable sugars, thus holding great potential in reducing the cost of the next-generation biofuels. Cellulase production is subject to induction by the presence of plant biomass components and to repression by the availability of easily metabolized sugars, such as glucose. Genes required for repression of cellulase gene expression when preferred carbon sources are present (carbon catabolite repression) and those that play a role in mediating glucose sensing/metabolism have been identified in filamentous fungi, but the mechanisms involved in crosstalk between repression versus induction of cellulase gene expression is poorly understood. Here, we report the identification and functional characterization of VIB1, a transcription factor essential for plant cell wall deconstruction in Neurospora crassa and COL26, a transcription factor that functions in glucose sensing/metabolism and regulation of CCR. We show that disabling CRE1 repression and modulating the glucose response by deletion of col-26 restored growth of the Δvib-1 mutant on cellulose. Our findings are particularly important in understanding the molecular basis of enzyme production that could allow a further strain improvement for plant biomass deconstruction.


Vyšlo v časopise: VIB1, a Link between Glucose Signaling and Carbon Catabolite Repression, Is Essential for Plant Cell Wall Degradation by. PLoS Genet 10(8): e32767. doi:10.1371/journal.pgen.1004500
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004500

Souhrn

Many filamentous fungi that grow on plant biomass are capable of producing lignocellulase enzymes to break down plant cell walls into utilizable sugars, thus holding great potential in reducing the cost of the next-generation biofuels. Cellulase production is subject to induction by the presence of plant biomass components and to repression by the availability of easily metabolized sugars, such as glucose. Genes required for repression of cellulase gene expression when preferred carbon sources are present (carbon catabolite repression) and those that play a role in mediating glucose sensing/metabolism have been identified in filamentous fungi, but the mechanisms involved in crosstalk between repression versus induction of cellulase gene expression is poorly understood. Here, we report the identification and functional characterization of VIB1, a transcription factor essential for plant cell wall deconstruction in Neurospora crassa and COL26, a transcription factor that functions in glucose sensing/metabolism and regulation of CCR. We show that disabling CRE1 repression and modulating the glucose response by deletion of col-26 restored growth of the Δvib-1 mutant on cellulose. Our findings are particularly important in understanding the molecular basis of enzyme production that could allow a further strain improvement for plant biomass deconstruction.


Zdroje

1. HimmelME, DingSY, JohnsonDK, AdneyWS, NimlosMR, et al. (2007) Biomass recalcitrance: engineering plants and enzymes for biofuels production. Science 315: 804–807.

2. LiuG, ZhangL, QinY, ZouG, LiZ, et al. (2013) Long-term strain improvements accumulate mutations in regulatory elements responsible for hyper-production of cellulolytic enzymes. Sci Rep 3: 1569.

3. KubicekCP, MikusM, SchusterA, SchmollM, SeibothB (2009) Metabolic engineering strategies for the improvement of cellulase production by Hypocrea jecorina. Biotechnol Biofuels 2: 19.

4. van PeijNN, GielkensMM, de VriesRP, VisserJ, de GraaffLH (1998) The transcriptional activator XlnR regulates both xylanolytic and endoglucanase gene expression in Aspergillus niger. Appl Environ Microbiol 64: 3615–3619.

5. GielkensMM, DekkersE, VisserJ, de GraaffLH (1999) Two cellobiohydrolase-encoding genes from Aspergillus niger require D-xylose and the xylanolytic transcriptional activator XlnR for their expression. Appl Environ Microbiol 65: 4340–4345.

6. StrickerAR, Grosstessner-HainK, WurleitnerE, MachRL (2006) Xyr1 (xylanase regulator 1) regulates both the hydrolytic enzyme system and D-xylose metabolism in Hypocrea jecorina. Eukaryot Cell 5: 2128–2137.

7. StrickerAR, MachRL, de GraaffLH (2008) Regulation of transcription of cellulases- and hemicellulases-encoding genes in Aspergillus niger and Hypocrea jecorina (Trichoderma reesei). Appl Microbiol Biotechnol 78: 211–220.

8. CoradettiST, CraigJP, XiongY, ShockT, TianC, et al. (2012) Conserved and essential transcription factors for cellulase gene expression in ascomycete fungi. Proc Natl Acad Sci U S A 109: 7397–7402.

9. ZnameroskiEA, CoradettiST, RocheCM, TsaiJC, IavaroneAT, et al. (2012) Induction of lignocellulose-degrading enzymes in Neurospora crassa by cellodextrins. Proc Natl Acad Sci U S A 109: 6012–6017.

10. CoradettiST, XiongY, GlassNL (2013) Analysis of a conserved cellulase transcriptional regulator reveals inducer-independent production of cellulolytic enzymes in Neurospora crassa. Microbiologyopen 2: 595–609.

11. OgawaM, KobayashiT, KoyamaY (2013) ManR, a transcriptional regulator of the beta-mannan utilization system, controls the cellulose utilization system in Aspergillus oryzae. Biosci Biotechnol Biochem 77: 426–429.

12. YamakawaY, EndoY, LiN, YoshizawaM, AoyamaM, et al. (2013) Regulation of cellulolytic genes by McmA, the SRF-MADS box protein in Aspergillus nidulans. Biochem Biophys Res Commun 431: 777–782.

13. KunitakeE, TaniS, SumitaniJ, KawaguchiT (2013) A novel transcriptional regulator, ClbR, controls the cellobiose- and cellulose-responsive induction of cellulase and xylanase genes regulated by two distinct signaling pathways in Aspergillus aculeatus. Appl Microbiol Biotechnol 97: 2017–2028.

14. AroN, SaloheimoA, IlmenM, PenttilaM (2001) ACEII, a novel transcriptional activator involved in regulation of cellulase and xylanase genes of Trichoderma reesei. J Biol Chem 276: 24309–24314.

15. NittaM, FurukawaT, ShidaY, MoriK, KuharaS, 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.

16. IlmenM, SaloheimoA, OnnelaML, PenttilaME (1997) Regulation of cellulase gene expression in the filamentous fungus Trichoderma reesei. Appl Environ Microbiol 63: 1298–1306.

17. AroN, PakulaT, PenttilaM (2005) Transcriptional regulation of plant cell wall degradation by filamentous fungi. FEMS Microbiol Rev 29: 719–739.

18. de VriesRP, VisserJ, de GraaffLH (1999) CreA modulates the XlnR-induced expression on xylose of Aspergillus niger genes involved in xylan degradation. Res Microbiol 150: 281–285.

19. OrejasM, MacCabeAP, Perez GonzalezJA, KumarS, RamonD (1999) Carbon catabolite repression of the Aspergillus nidulans xlnA gene. Mol Microbiol 31: 177–184.

20. OrejasM, MacCabeAP, Perez-GonzalezJA, KumarS, RamonD (2001) The wide-domain carbon catabolite repressor CreA indirectly controls expression of the Aspergillus nidulans xlnB gene, encoding the acidic endo-beta-(1,4)-xylanase X(24). J Bacteriol 183: 1517–1523.

21. BaileyC, ArstHNJr (1975) Carbon catabolite repression in Aspergillos nidulans. Eur J Biochem 51: 573–577.

22. ShroffRA, O'ConnorSM, HynesMJ, LockingtonRA, KellyJM (1997) Null alleles of creA, the regulator of carbon catabolite repression in Aspergillus nidulans. Fungal Genet Biol 22: 28–38.

23. StraussJ, MachRL, ZeilingerS, HartlerG, StofflerG, et al. (1995) Cre1, the carbon catabolite repressor protein from Trichoderma reesei. FEBS Lett 376: 103–107.

24. TakashimaS, IikuraH, NakamuraA, MasakiH, UozumiT (1996) Analysis of Cre1 binding sites in the Trichoderma reesei cbh1 upstream region. FEMS Microbiol Lett 145: 361–366.

25. IlmenM, ThraneC, PenttilaM (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.

26. SunJ, GlassNL (2011) Identification of the CRE-1 cellulolytic regulon in Neurospora crassa. PLoS One 6: e25654.

27. ZivC, GorovitsR, YardenO (2008) Carbon source affects PKA-dependent polarity of Neurospora crassa in a CRE-1-dependent and independent manner. Fungal Genet Biol 45: 103–116.

28. TamayoEN, VillanuevaA, HasperAA, de GraaffLH, RamonD, 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.

29. FlipphiM, van de VondervoortPJ, RuijterGJ, VisserJ, ArstHNJr, et al. (2003) Onset of carbon catabolite repression in Aspergillus nidulans. Parallel involvement of hexokinase and glucokinase in sugar signaling. J Biol Chem 278: 11849–11857.

30. ToddRB, LockingtonRA, KellyJM (2000) The Aspergillus nidulans creC gene involved in carbon catabolite repression encodes a WD40 repeat protein. Mol Gen Genet 263: 561–570.

31. LockingtonRA, KellyJM (2001) Carbon catabolite repression in Aspergillus nidulans involves deubiquitination. Mol Microbiol 40: 1311–1321.

32. LockingtonRA, KellyJM (2002) The WD40-repeat protein CreC interacts with and stabilizes the deubiquitinating enzyme CreB in vivo in Aspergillus nidulans. Mol Microbiol 43: 1173–1182.

33. BoaseNA, KellyJM (2004) A role for creD, a carbon catabolite repression gene from Aspergillus nidulans, in ubiquitination. Mol Microbiol 53: 929–940.

34. DentonJA, KellyJM (2011) Disruption of Trichoderma reesei cre2, encoding an ubiquitin C-terminal hydrolase, results in increased cellulase activity. BMC Biotechnol 11: 103.

35. ZhouG, LuJ, LiZ, LiJ, WangM, et al. (2012) Enhanced cellulase production of Penicillium decumbens by knocking out CreB encoding a deubiquitination enzyme [Chinese]. Sheng Wu Gong Cheng Xue Bao 28: 959–972.

36. GremelG, DorrerM, SchmollM (2008) Sulphur metabolism and cellulase gene expression are connected processes in the filamentous fungus Hypocrea jecorina (anamorph Trichoderma reesei). BMC Microbiol 8: 174.

37. AroN, IlmenM, SaloheimoA, PenttilaM (2003) ACEI of Trichoderma reesei is a repressor of cellulase and xylanase expression. Appl Environ Microbiol 69: 56–65.

38. EbboleDJ (1998) Carbon catabolite repression of gene expression and conidiation in Neurospora crassa. Fungal Genetics and Biology 25: 15–21.

39. MadiL, McBrideSA, BaileyLA, EbboleDJ (1997) rco-3, a gene involved in glucose transport and conidiation in Neurospora crassa. Genetics 146: 499–508.

40. BrownNA, de GouveaPF, KrohnNG, SavoldiM, GoldmanGH (2013) Functional characterisation of the non-essential protein kinases and phosphatases regulating Aspergillus nidulans hydrolytic enzyme production. Biotechnol Biofuels 6: 91.

41. FernandezJ, WrightJD, HartlineD, QuispeCF, MadayiputhiyaN, et al. (2012) Principles of carbon catabolite repression in the rice blast fungus: Tps1, Nmr1-3, and a MATE-family pump regulate glucose metabolism during infection. PLoS Genet 8: e1002673.

42. DavisRH, PerkinsDD (2002) Timeline: Neurospora: a model of model microbes. Nat Rev Genet 3: 397–403.

43. TurnerBC, PerkinsDD, FairfieldA (2001) Neurospora from natural populations: a global study. Fungal Genet Biol 32: 67–92.

44. TianC, BeesonWT, IavaroneAT, SunJ, MarlettaMA, 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.

45. PhillipsCM, IavaroneAT, MarlettaMA (2011) Quantitative proteomic approach for cellulose degradation by Neurospora crassa. J Proteome Res 10: 4177–4185.

46. ColotHV, ParkG, TurnerGE, RingelbergC, CrewCM, 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.

47. XiangQ, GlassNL (2002) Identification of vib-1, a locus involved in vegetative incompatibility mediated by het-c in Neurospora crassa. Genetics 162: 89–101.

48. DementhonK, IyerG, GlassNL (2006) VIB-1 is required for expression of genes necessary for programmed cell death in Neurospora crassa. Eukaryot Cell 5: 2161–2173.

49. HutchisonEA, BuecheJA, GlassNL (2012) Diversification of a protein kinase cascade: IME-2 is involved in nonself recognition and programmed cell death in Neurospora crassa. Genetics 192: 467–482.

50. McCluskeyK (2003) The Fungal Genetics Stock Center: from molds to molecules. Adv Appl Microbiol 52: 245–262.

51. LombardV, Golaconda RamuluH, DrulaE, CoutinhoPM, HenrissatB (2013) The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res 42: D490–495.

52. GlassNL, SchmollM, CateJH, CoradettiS (2013) Plant cell wall deconstruction by ascomycete fungi. Annu Rev Microbiol 67: 477–498.

53. GalazkaJM, TianC, BeesonWT, MartinezB, GlassNL, et al. (2010) Cellodextrin transport in yeast for improved biofuel production. Science 330: 84–86.

54. XiongY, CoradettiST, LiX, GritsenkoMA, ClaussT, et al. (2014) The proteome and phosphoproteome of Neurospora crassa in response to cellulose, sucrose and carbon starvation. Fungal Genet Biol (in press).

55. EveleighDE, MontenecourtBS (1979) Increasing yields of extracellular enzymes. Adv Appl Microbiol 25: 57–74.

56. SheirneissG, MontenecourtBS (1984) Characterization of the secreted cellulases of Trichoderma reesei wild type and mutants during controlled fermentations. Appl Microbiol Biotechnol 20: 46–53.

57. AllenKE, McNallyMT, LowendorfHS, SlaymanCW, FreeSJ (1989) Deoxyglucose-resistant mutants of Neurospora crassa: isolation, mapping, and biochemical characterization. J Bacteriol 171: 53–58.

58. XieX, WilkinsonHH, CorreaA, LewisZA, Bell-PedersenD, et al. (2004) Transcriptional response to glucose starvation and functional analysis of a glucose transporter of Neurospora crassa. Fungal Genet Biol 41: 1104–1119.

59. DelmasS, PullanST, GaddipatiS, KokolskiM, MallaS, et al. (2012) Uncovering the genome-wide transcriptional responses of the filamentous fungus Aspergillus niger to lignocellulose using RNA sequencing. PLoS Genet 8: e1002875.

60. RollandF, WinderickxJ, TheveleinJM (2002) Glucose-sensing and -signalling mechanisms in yeast. FEMS Yeast Res 2: 183–201.

61. GancedoJM (1998) Yeast carbon catabolite repression. Microbiol Mol Biol Rev 62: 334–361.

62. LimonMC, PakulaT, SaloheimoM, PenttilaM (2011) The effects of disruption of phosphoglucose isomerase gene on carbon utilisation and cellulase production in Trichoderma reesei Rut-C30. Microbial Cell Factories 10: 40.

63. Porciuncula JdeO, FurukawaT, MoriK, ShidaY, HirakawaH, et al. (2013) Single nucleotide polymorphism analysis of a Trichoderma reesei hyper-cellulolytic mutant developed in Japan. Biosci Biotechnol Biochem 77: 534–543.

64. Le CromS, SchackwitzW, PennacchioL, MagnusonJK, CulleyDE, et al. (2009) Tracking the roots of cellulase hyperproduction by the fungus Trichoderma reesei using massively parallel DNA sequencing. Proc Natl Acad Sci U S A 106: 16151–16156.

65. VitikainenM, ArvasM, PakulaT, OjaM, PenttilaM, et al. (2010) Array comparative genomic hybridization analysis of Trichoderma reesei strains with enhanced cellulase production properties. BMC Genomics 11: 441.

66. KatzME, FlynnPK, vanKuykPA, CheethamBF (1996) Mutations affecting extracellular protease production in the filamentous fungus Aspergillus nidulans. Mol Gen Genet 250: 715–724.

67. KatzME, BernardoSM, CheethamBF (2008) The interaction of induction, repression and starvation in the regulation of extracellular proteases in Aspergillus nidulans: evidence for a role for CreA in the response to carbon starvation. Curr Genet 54: 47–55.

68. KatzME, GrayKA, CheethamBF (2006) The Aspergillus nidulans xprG (phoG) gene encodes a putative transcriptional activator involved in the response to nutrient limitation. Fungal Genet Biol 43: 190–199.

69. BernardoSM, GrayKA, ToddRB, CheethamBF, KatzME (2007) Characterization of regulatory non-catalytic hexokinases in Aspergillus nidulans. Mol Genet Genomics 277: 519–532.

70. HutchisonEA, GlassNL (2010) Meiotic regulators Ndt80 and ime2 have different roles in Saccharomyces and Neurospora. Genetics 185: 1271–1282.

71. RicciM, KrappmannD, RussoVEA (1991) Nitrogen and carbon starvation regulate conidia and protoperithecia formation in Neurospora crassa grown on solid media. Fungal Genet Newslett 38: 87–88.

72. XiangQ, GlassNL (2004) The control of mating type heterokaryon incompatibility by vib-1, a locus involved in het-c heterokaryon incompatibility in Neurospora crassa. Fungal Genet Biol 41: 1063–1076.

73. KatzME, BraunbergerK, YiG, CooperS, NonhebelHM, et al. (2013) A p53-like transcription factor similar to Ndt80 controls the response to nutrient stress in the filamentous fungus, Aspergillus nidulans. F1000Res 2: 72.

74. WhiteS, McIntyreM, BerryDR, McNeilB (2002) The autolysis of industrial filamentous fungi. Crit Rev Biotechnol 22: 1–14.

75. Puzio-KuterAM (2011) The role of p53 in metabolic regulation. Genes Cancer 2: 385–391.

76. MaddocksOD, VousdenKH (2011) Metabolic regulation by p53. J Mol Med 89: 237–245.

77. AramayoR, MetzenbergRL (1996) Gene replacements at the his-3 locus of Neurospora crassa. Fungal Genet Newsl 43: 9–13.

78. VogelH (1956) A convenient growth medium for Neurospora. Microb Genet Bull 13: 2–43.

79. WestergaardM, MitchellHK (1947) Neurospora V. A synthetic medium favoring sexual reproduction. Am J Botany 34: 573–577.

80. DavisRH, SerresFJd (1970) Genetic and microbiological research techniques for Neurospora crassa. Meth Enzymol 17: 79–143.

81. GalaganJE, CalvoSE, BorkovichKA, SelkerEU, ReadND, et al. (2003) The genome sequence of the filamentous fungus Neurospora crassa. Nature 422: 859–868.

82. LangmeadB, TrapnellC, PopM, SalzbergSL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25.

83. TrapnellC, RobertsA, GoffL, PerteaG, KimD, et al. (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7: 562–578.

84. de HoonMJ, ImotoS, NolanJ, MiyanoS (2004) Open source clustering software. Bioinformatics 20: 1453–1454.

85. RueppA, ZollnerA, MaierD, AlbermannK, HaniJ, et al. (2004) The FunCat, a functional annotation scheme for systematic classification of proteins from whole genomes. Nucleic Acids Res 32: 5539–5545.

86. LiuH, OsmaniAH, UkilL, SonS, MarkossianS, et al. (2010) Single-step affinity purification for Fungal Proteomics. Eukayot Cell 9: 831–833.

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