Skip to main content
Log in

Interactome analysis of transcriptional coactivator multiprotein bridging factor 1 unveils a yeast AP-1-like transcription factor involved in oxidation tolerance of mycopathogen Beauveria bassiana

  • Original Article
  • Published:
Current Genetics Aims and scope Submit manuscript

Abstract

Oxidation tolerance is an important determinant to predict the virulence and biocontrol potential of Beauveria bassiana, a well-known entomopathogenic fungus. As a transcriptional coactivator, multiprotein bridging factor 1 mediates the activity of transcription factor in diverse physiological processes, and its homolog in B. bassiana (BbMBF1) contributes to fungal oxidation tolerance. In this study, the BbMBF1-interactomes under oxidative stress and normal growth condition were deciphered by mass spectrometry integrated with the immunoprecipitation. BbMBF1p factor has a broad interaction with proteins that are involved in various cellular processes, and this interaction is dynamically regulated by oxidative stress. Importantly, a B. bassiana homolog of yeast AP-1-like transcription factor (BbAP-1) was specifically associated with the BbMBF1-interactome under oxidation and significantly contributed to fungal oxidation tolerance. In addition, qPCR analysis revealed that several antioxidant genes are jointly controlled by BbAP-1 and BbMBF1. Conclusively, it is proposed that BbMBF1p protein mediates BbAP-1p factor to transcribe the downstream antioxidant genes in B. bassiana under oxidative stress. This study demonstrates for the first time a proteomic view of the MBF1-interactome in fungi, and presents an initial framework to probe the transcriptional mechanism involved in fungal response to oxidation, which will provide a new strategy to improve the biocontrol efficacy of B. bassiana.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abdalla KO, Thomson JA, Rafudeen MS (2009) Protocols for nuclei isolation and nuclear protein extraction from the resurrection plant Xerophyta viscosa for proteomic studies. Anal Biochem 384:365–367

    Article  CAS  PubMed  Google Scholar 

  • Azevedo RF, Souza RK, Braga GU, Rangel DE (2014) Responsiveness of entomopathogenic fungi to menadione-induced oxidative stress. Fungal Biol 118:990–995

    Article  CAS  PubMed  Google Scholar 

  • Brendel C, Gelman L, Auwerx J (2002) Multiprotein bridging factor-1 (MBF-1) is a cofactor for nuclear receptors that regulate lipid metabolism. Mol Endocrinol 16:1367–1377

    Article  CAS  PubMed  Google Scholar 

  • Chu XL, Feng MG, Ying SH (2015) Transcriptomic analysis reveals the potential antioxidant pathways regulated by multiprotein bridging factor 1 (BbMBF1) in the fungal entomopathogen Beauveria bassiana. Biocontrol Sci Technol 25:1346–1358

    Article  Google Scholar 

  • Coto JM, Ehrenhofer-Murray AE, Pons T, Siebers B (2011) Functional analysis of archaeal MBF1 by complementation studies in yeast. Biol Direct 6:18

    Article  CAS  Google Scholar 

  • Gauci S, Veenhoff LM, Heck AJR, Krijgsveld J (2009) Orthogonal separation techniques for the characterization of the yeast nuclear proteome. J Proteome Res 8:3451–3463

    Article  CAS  PubMed  Google Scholar 

  • Ge F, Li WL, Bi LJ, Tao SC, Zhang ZP, Zhang XE (2010) Identification of novel 14-3-3 interacting proteins by quantitative immunoprecipitation combined with knockdown (QUICK). J Proteome Res 9:5848–5858

    Article  CAS  PubMed  Google Scholar 

  • Guo M, Chen Y, Du Y, Dong Y, Guo W, Zhai S, Zhang H, Dong S, Zhang Z, Wang Y, Wang P, Zheng X (2011) The bZIP transcription factor MoAP1 mediates the oxidative stress response and is critical for pathogenicity of the rice blast fungus Magnaporthe oryzae. PLoS Pathog 7:e1001302

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hautala JA, Conner BH, Jacobson JW, Patel GL, Giles NH (1977) Isolation and characterization of nuclei from Neurospora crassa. J Bacteriol 130:704–713

    CAS  PubMed  PubMed Central  Google Scholar 

  • He PH, Dong WX, Chu XL, Feng MG, Ying SH (2016) The cellular proteome is affected by a gelsolin (BbGEL1) during morphological transitions in aerobic surface versus liquid growth in the entomopathogenic fungus Beauveria bassiana. Environ Microbiol 18:4153–4169

    Article  CAS  PubMed  Google Scholar 

  • Hillmann F, Shekhova E, Kniemeyer O (2015) Insights into the cellular responses to hypoxia in filamentous fungi. Curr Genet 61:441–455

    Article  CAS  PubMed  Google Scholar 

  • Huarte-Bonnet C, Juárez MP, Pedrini N (2015) Oxidative stress in entomopathogenic fungi grown on insect-like hydrocarbons. Curr Genet 61:289–297

    Article  CAS  PubMed  Google Scholar 

  • Ingolia NT, Ghaemmaghami S, Newman JRS, Weissman JS (2009) Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science 324:218–223

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jaszek M, Żuchowski J, Dajczak E, Cimek K, Gra̢z M, Grzywnowicz K (2006) Ligninolytic enzymes can participate in a multiple response system to oxidative stress in white-rot basidiomycetes: Fomes fomentarius and Tyromyces pubescens. Int Biodeter Biodegr 58:168–175

    Article  CAS  Google Scholar 

  • Kabe Y, Goto M, Shina D, Imai T, Wada T, Morohashi KI, Shirakawa M, Hirose S, Handa H (1999) The role of human MBF1 as a transcriptional co-activator. J Biol Chem 274:34196–34202

    Article  CAS  PubMed  Google Scholar 

  • Li Q, Abrashev R, Harvey LM, McNeil B (2008) Oxidative stress-associated impairment of glucose and ammonia metabolism in the filamentous fungus, Aspergillus niger B1-D. Mycol Res 112:1049–1055

    Article  CAS  PubMed  Google Scholar 

  • Li F, Shi HQ, Ying SH, Feng MG (2015) Distinct contributions of one Fe- and two Cu/Zn-cofactored superoxide dismutases to antioxidation, UV tolerance and virulence of Beauveria bassiana. Fungal Genet Biol 81:160–171

    Article  CAS  PubMed  Google Scholar 

  • Liu Q, Ying SH, Li JG, Tian CG, Feng MG (2013) Insight into the transcriptional regulation of Msn2 required for conidiation, multi-stress responses and virulence of two entomopathogenic fungi. Fungal Genet Biol 54:42–51

    Article  CAS  PubMed  Google Scholar 

  • Liu Q, Li JG, Ying SH, Wang JJ, Sun WL, Tian CG, Feng MG (2015) Unveiling equal importance of two 14-3-3 proteins for morphogenesis, conidiation, stress tolerance and virulence of an insect pathogen. Environ Microbiol 17:1444–1462

    Article  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Molina L, Kahmann R (2007) An Ustilago maydis gene involved in H2O2 detoxification is required for virulence. Plant Cell 19:2293–2309

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moye-Rowley WS (2003) Regulation of the transcriptional response to oxidative stress in fungi: similarities and differences. Eukaryot Cell 2:381–389

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moye-Rowley WS, Harshman KD, Parker CS (1989) Yeast YAP1 encodes a novel form of the jun family of transcriptional activator proteins. Genes Dev 3:283–292

    Article  CAS  PubMed  Google Scholar 

  • Ortiz-Urquiza A, Keyhani NO (2015) Stress response signaling and virulence: insights from entomopathogenic fungi. Curr Genet 61:239–249

    Article  CAS  PubMed  Google Scholar 

  • Rangel D, Braga GUL, Fernandes ÉKK, Keyser CA, Hallsworth JE, Roberts DW (2015) Stress tolerance and virulence of insect-pathogenic fungi are determined by environmental conditions during conidial formation. Curr Genet 61:383–404

    Article  CAS  PubMed  Google Scholar 

  • Rehner SA, Minnis AM, Sung G, Luangsa-ard JJ, Devotto L, Humber RA (2011) Phylogeny and systematics of the anamorphic, entomopathogenic genus Beauveria. Mycologia 103:1055–1073

    Article  PubMed  Google Scholar 

  • Rodrigues-Pousada C, Menezes RA, Pimentel C (2010) The Yap family and its role in stress response. Yeast 27:245–258

    Article  CAS  PubMed  Google Scholar 

  • Ruepp A, Zollner A, Maier D, Albermann K, Hani J, Mokrejs M, Tetko I, Güldener U, Mannhaupt G, Münsterkötter M, Mewes HW (2004) The FunCat, a functional annotation scheme for systematic classification of proteins from whole genomes. Nucleic Acids Res 32:5539–5545

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shalaby S, Horwitz BA (2015) Plant phenolic compounds and oxidative stress: integrated signals in fungal–plant interactions. Curr Genet 61:347–357

    Article  CAS  PubMed  Google Scholar 

  • Shelest E (2008) Transcription factors in fungi. FEMS Microbiol Lett 286:145–151

    Article  CAS  PubMed  Google Scholar 

  • Song C, Ortiz-Urquiza A, Ying SH, Zhang JX, Keyhani NO (2015) Interaction between TATA-binding protein (TBP) and multiprotein bridging factor-1 (MBF1) from the filamentous insect pathogenic fungus Beauveria bassiana. PLoS One 10:e0140538

    Article  PubMed  PubMed Central  Google Scholar 

  • St. Leger RJ, Wang C (2010) Genetic engineering of fungal biocontrol agents to achieve greater efficacy against insect pests. Appl Microbiol Biotechnol 85:901–907

    Article  CAS  PubMed  Google Scholar 

  • Stephen DW, Rivers SL, Jamieson DJ (1995) The role of the YAP1 and YAP2 genes in the regulation of the adaptive oxidative stress responses of Saccharomyces cerevisiae. Mol Microbiol 16:415–423

    Article  CAS  PubMed  Google Scholar 

  • Sun Y, Wang Y, Tian C (2016) bZIP transcription factor CgAP1 is essential for oxidative stress tolerance and full virulence of the poplar anthracnose fungus Colletotrichum gloeosporioides. Fungal Genet Biol 95:58–66

    Article  CAS  PubMed  Google Scholar 

  • Suzuki N, Sejima H, Tam R, Schlauch K, Mittler R (2011) Identification of the MBF1 heat-response regulon of Arabidopsis thaliana. Plant J 66:844–851

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takahashi M, Yamashita K, Shiozawa A, Ichiishi A, Fukumori F, Fujimura M (2010) An AP-1-like transcription tactor, NAP-1, regulates expression of the glutathione S-transferase and NADH: flavin oxidoreductase genes in Neurospora crassa. Biosci Biotechnol Biochem 74:746–752

    Article  CAS  PubMed  Google Scholar 

  • Takemaru K, Li FQ, Ueda H, Hirose S (1997) Multiprotein bridging factor 1 (MBF1) is an evolutionarily conserved transcriptional coactivator that connects a regulatory factor and TATA element-binding protein. Proc Natl Acad Sci USA 94:7251–7256

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takemaru K, Harashima S, Ueda H, Hirose S (1998) Yeast co-activator MBF1 mediates GCN4-dependent transcriptional activation. Mol Cell Biol 18:4971–4976

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tamayo D, Muñoz JF, Torres I, Almeida AJ, Restrepo A, McEwen JG, Hernández O (2013) Involvement of the 90 kDa heat shock protein during adaptation of Paracoccidioides brasiliensis to different environmental conditions. Fungal Genet Biol 51:34–41

    Article  CAS  PubMed  Google Scholar 

  • Toone WM, Jones N (1998) Stress-activated signalling pathways in yeast. Genes Cells 3:485–498

    Article  CAS  PubMed  Google Scholar 

  • Vizcaíno JA, Deutsch EW, Wang R, Csordas A, Reisinger F, Ríos D, Dianes JA, Sun Z, Farrah T, Bandeira N, Binz PA, Xenarios I, Eisenacher M, Mayer G, Gatto L, Campos A, Chalkley RJ, Kraus HJ, Albar JP, Martinez-Bartolomé S, Apweiler R, Omenn GS, Martens L, Jones AR, Hermjakob H (2014) ProteomeXchange provides globally co-ordinated proteomics data submission and dissemination. Nat Biotechnol 30:223–226

    Article  Google Scholar 

  • Wang ZL, Zhang LB, Ying SH, Feng MG (2012) Primary roles of two dehydrogenases in the mannitol metabolism and multi-stress tolerance of entomopathogenic fungus Beauveria bassiana. Environ Microbiol 14:2139–2150

    Article  CAS  PubMed  Google Scholar 

  • Wang ZL, Zhang LB, Ying SH, Feng MG (2013) Catalases play differentiated roles in the adaptation of a fungal entomopathogen to environmental stresses. Environ Microbiol 15:409–418

    Article  CAS  PubMed  Google Scholar 

  • Xie XQ, Li F, Ying SH, Feng MG (2012) Additive contributions of two manganese-cored superoxide dismutases (MnSODs) to antioxidation, UV tolerance and virulence of Beauveria bassiana. PLoS One 7:e30298

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang Y, Fan F, Zhuo R, Ma F, Gong Y, Wan X, Jiang M, Zhang X (2012) Expression of the laccase gene from a white rot fungus in Pichia pastoris can enhance the resistance of this yeast to H2O2-mediated oxidative stress by stimulating the glutathione-based antioxidative system. Appl Environ Microbiol 78:5845–5854

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ying SH, Feng MG, Keyhani NO (2013) A carbon responsive G-protein coupled receptor modulates broad developmental and genetic networks in the entomopathogenic fungus, Beauveria bassiana. Environ Microbiol 15:2902–2921

    CAS  PubMed  Google Scholar 

  • Ying SH, Ji XP, Wang XX, Feng MG, Keyhani NO (2014) The transcriptional co-activator multiprotein bridging factor 1 from the fungal insect pathogen, Beauveria bassiana, mediates regulation of hyphal morphogenesis, stress tolerance and virulence. Environ Microbiol 16:1879–1897

    Article  CAS  PubMed  Google Scholar 

  • Ying SH, Liu J, Chu XL, Xie XQ, Feng MG (2016) The autophagy-related genes BbATG1 and BbATG8 have different functions in differentiation, stress resistance and virulence of mycopathogen Beauveria bassiana. Sci Rep 6:26376

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zanetti ME, Chan RL, Godoy AV, González DH, Casalongué CA (2004) Homeodomain-leucine zipper proteins interact with a plant homologue of the transcriptional co-activator multiprotein bridging factor 1. J Biochem Mol Biol 37:320–324

    CAS  PubMed  Google Scholar 

  • Zlatic SA, Ryder PV, Salazar G, Faundez V (2010) Isolation of labile multi-protein complexes by in vivo controlled cellular cross-linking and immuno-magnetic affinity chromatography. J Vis Exp 37:1855

    Google Scholar 

Download references

Acknowledgements

This study was jointly supported by the National Key R&D Program of China (2017YFD0200400) and the National Natural Science Foundation of China (31171898).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sheng-Hua Ying.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by M. Kupiec.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 319 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chu, XL., Dong, WX., Ding, JL. et al. Interactome analysis of transcriptional coactivator multiprotein bridging factor 1 unveils a yeast AP-1-like transcription factor involved in oxidation tolerance of mycopathogen Beauveria bassiana . Curr Genet 64, 275–284 (2018). https://doi.org/10.1007/s00294-017-0741-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00294-017-0741-4

Keywords

Navigation