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Comparative transcriptomics and transcriptional regulation analysis of enhanced laccase production induced by co-culture of Pleurotus eryngii var. ferulae with Rhodotorula mucilaginosa

  • Qi Zhang
  • Liting Zhao
  • YouRan Li
  • Feng Wang
  • Song Li
  • Guiyang Shi
  • Zhongyang DingEmail author
Genomics, transcriptomics, proteomics
  • 117 Downloads

Abstract

The co-culturing of Pleurotus eryngii var. ferulae and Rhodotorula mucilaginosa was confirmed in our previous studies to be an efficient strategy to improve laccase production by submerged fermentation. To determine the possible regulation principles underlying this behaviour, comparative transcriptomic analysis was performed on P. eryngii var. ferulae to investigate the differential expression of genes in co-culture. RNA-seq analysis showed that genes concerning xenobiotic biodegradation and expenditure of energy were upregulated. However, genes related to oxidative stress were downregulated. In addition, the transcription levels of laccase isoenzymes were not consistent in the co-culture system: 3 laccase genes (lacc1, lacc2, lacc12) were upregulated, and 3 laccase genes (lacc4, lacc6, lacc9) were downregulated. The enhancement in laccase activity can be due to upregulation of a laccase heterodimer encoded by the genes lacc2 and ssPOXA3a (or ssPOXA3b), whose expression levels were increased by 459% and 769% (or 585% for ssPOXA3b) compared with those of a control, respectively. β-Carotene produced by R. mucilaginosa upregulated the transcription of lacc2 only. Combining these results with an analysis of cis-acting responsive elements indicated that four transcription factors (TFs) had potential regulatory effects on the transcription of laccase genes. It was supposed that TFa regulated lacc transcription by binding with methyl jasmonate and heat shock response elements. The expression of TFb, TFc, and TFd was regulated by β-carotene. However, β-carotene had no effect on TFa expression. These results provide a possible mechanism for the regulation of laccase gene transcription in the co-culture system and are also beneficial for the future intensification of fungal laccase production.

Keywords

Laccase Co-culture β-Carotene RNA-seq Transcriptional regulation 

Notes

Acknowledgments

Funding for this study was provided by the National Natural Science Foundation of China (31571822) and the Science and Technology Project of Jiangsu Province (social development category, BE2017683). This study was also sponsored by the National First-Class Discipline Programme of Light Industry Technology and Engineering (LITE2018-22).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Informed consent

This research did not involve any human participants.

Supplementary material

253_2019_10228_MOESM1_ESM.pdf (765 kb)
ESM 1 (PDF 765 kb)

References

  1. Alfaro M, Castanera R, Lavín JL, Grigoriev IV, Oguiza JA, Ramírez L, Pisabarro AG (2016) Comparative and transcriptional analysis of the predicted secretome in the lignocellulose-degrading basidiomycete fungus Pleurotus ostreatus. Environ Microbiol 18(12):4710–4726.  https://doi.org/10.1111/1462-2920.13360 CrossRefPubMedGoogle Scholar
  2. Asina F, Brzonova I, Voeller K, Kozliak E, Kubatova A, Yao B, Ji Y (2016) Biodegradation of lignin by fungi, bacteria and laccases. Bioresour Technol 220:414–424.  https://doi.org/10.1016/j.biortech.2016.08.016 CrossRefPubMedGoogle Scholar
  3. Badis G, Chan ET, van Bakel H, Pena-Castillo L, Tillo D, Tsui K, Carlson CD, Gossett AJ, Hasinoff MJ, Warren CL, Gebbia M, Talukder S, Yang A, Mnaimneh S, Terterov D, Coburn D, Li Yeo A, Yeo ZX, Clarke ND, Lieb JD, Ansari AZ, Nislow C, Hughes TR (2008) A library of yeast transcription factor motifs reveals a widespread function for Rsc3 in targeting nucleosome exclusion at promoters. Mol Cell 32(6):878–887.  https://doi.org/10.1016/j.molcel.2008.11.020 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Balderas-Hernandez VE, Correia K, Mahadevan R (2018) Inactivation of the transcription factor mig1 (YGL035C) in Saccharomyces cerevisiae improves tolerance towards monocarboxylic weak acids: acetic, formic and levulinic acid. J Ind Microbiol Biotechnol 45(8):735–751.  https://doi.org/10.1007/s10295-018-2053-1 CrossRefPubMedGoogle Scholar
  5. Castanera R, Perez G, Omarini A, Alfaro M, Pisabarro AG, Faraco V, Amore A, Ramírez L (2012) Transcriptional and enzymatic profiling of Pleurotus ostreatus laccase genes in submerged and solid-state fermentation cultures. Appl Environ Microbiol 78(11):4037–4045.  https://doi.org/10.1128/AEM.07880-11 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Castanera R, López-Varas L, Pisabarro AG, Ramírez L (2015) Validation of reference genes for transcriptional analyses in Pleurotus ostreatus by using reverse transcription-quantitative PCR. Appl Environ Microbiol 81(12):4120–4129.  https://doi.org/10.1128/AEM.00402-15 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Copete-Pertuz LS, Alandete-Novoa F, Placido J, Correa-Londono GA, Mora-Martinez AL (2019) Enhancement of ligninolytic enzymes production and decolourising activity in Leptosphaerulina sp. by co-cultivation with Trichoderma viride and Aspergillus terreus. Sci Total Environ 646:1536–1545.  https://doi.org/10.1016/j.scitotenv.2018.07.387 CrossRefPubMedGoogle Scholar
  8. Darwish WS, Ikenaka Y, Nakayama S, Mizukawa H, Thompson LA, Ishizuka M (2018) beta-Carotene and retinol reduce benzo[a]pyrene-induced mutagenicity and oxidative stress via transcriptional modulation of xenobiotic metabolizing enzymes in human HepG2 cell line. Environ Sci Pollut Res Int 25(7):6320–6328.  https://doi.org/10.1007/s11356-017-0977-z CrossRefPubMedGoogle Scholar
  9. Du W, Sun C, Wang J, Xie W, Wang B, Liu X, Zhang Y, Fan Y (2017) Conditions and regulation of mixed culture to promote Shiraia bambusicola and Phoma sp. BZJ6 for laccase production. Sci Rep 7(1):17801.  https://doi.org/10.1038/s41598-017-17895-w CrossRefPubMedPubMedCentralGoogle Scholar
  10. Fan F, Zhuo R, Sun S, Wan X, Jiang M, Zhang X, Yang Y (2011) Cloning and functional analysis of a new laccase gene from Trametes sp. 48424 which had the high yield of laccase and strong ability for decolorizing different dyes. Bioresour Technol 102(3):3126–3137.  https://doi.org/10.1016/j.biortech.2010.10.079 CrossRefPubMedGoogle Scholar
  11. Faraco V, Ercole C, Festa G, Giardina P, Piscitelli A, Sannia G (2008) Heterologous expression of heterodimeric laccase from Pleurotus ostreatus in Kluyveromyces lactis. Appl Microbiol Biotechnol 77(6):1329–1335.  https://doi.org/10.1007/s00253-007-1265-5 CrossRefPubMedGoogle Scholar
  12. Fischer CN, Trautman EP, Crawford JM, Stabb EV, Handelsman J, Broderick NA (2017) Metabolite exchange between microbiome members produces compounds that influence Drosophila behavior. Elife 6:e18855.  https://doi.org/10.7554/eLife.18855 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Flores C, Vidal C, Trejo-Hernandez MR, Galindo E, Serrano-Carreon L (2009) Selection of Trichoderma strains capable of increasing laccase production by Pleurotus ostreatus and Agaricus bisporus in dual cultures. J Appl Microbiol 106(1):249–257.  https://doi.org/10.1111/j.1365-2672.2008.03998.x CrossRefPubMedGoogle Scholar
  14. Giardina P, Sannia G (2015) Laccases: old enzymes with a promising future. Cell Mol Life Sci 72(5):855–856.  https://doi.org/10.1007/s00018-014-1821-y CrossRefPubMedGoogle Scholar
  15. Giardina P, Autore F, Faraco V, Festa G, Palmieri G, Piscitelli A, Sannia G (2007) Structural characterization of heterodimeric laccases from Pleurotus ostreatus. Appl Microbiol Biotechnol 75(6):1293–1300.  https://doi.org/10.1007/s00253-007-0954-4 CrossRefPubMedGoogle Scholar
  16. Goudopoulou A, Krimitzas A, Typas MA (2010) Differential gene expression of ligninolytic enzymes in Pleurotus ostreatus grown on olive oil mill wastewater. Appl Microbiol Biotechnol 88(2):541–551.  https://doi.org/10.1007/s00253-010-2750-9 CrossRefPubMedGoogle Scholar
  17. Grabherr M, Haas B, Yassour M, Levin J, Thompson D, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, Palma F, Birren B, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644–652.  https://doi.org/10.1038/nbt.1883 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Guo C, Zhao L, Wang F, Lu J, Ding Z, Shi G (2017) beta-Carotene from yeasts enhances laccase production of Pleurotus eryngii var. ferulae in co-culture. Front Microbiol 8:1101.  https://doi.org/10.3389/fmicb.2017.01101 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Hailei W, Guangli Y, Ping L, Yanchang G, Jun L, Guosheng L, Jianming Y (2009) Overproduction of Trametes versicolor laccase by making glucose starvation using yeast. Enzym Microb Tech 45(2):146–149.  https://doi.org/10.1016/j.enzmictec.2009.04.003 CrossRefGoogle Scholar
  20. Hoegger PJ, Kilaru S, James TY, Thacker JR, Kües U (2006) Phylogenetic comparison and classification of laccase and related multicopper oxidase protein sequences. FEBS J 273(10):2308–2326.  https://doi.org/10.1111/j.1742-4658.2006.05247.x CrossRefPubMedGoogle Scholar
  21. Hou H, Zhou J, Wang J, Du C, Yan B (2004) Enhancement of laccase production by Pleurotus ostreatus and its use for the decolorization of anthraquinone dye. Process Biochem 39(11):1415–1419.  https://doi.org/10.1016/s0032-9592(03)00267-x CrossRefGoogle Scholar
  22. Hu J, Zhang Y, Xu Y, Sun Q, Liu J, Fang W, Xiao Y, Kües U, Fang Z (2019) Gongronella sp. w5 elevates Coprinopsis cinerea laccase production by carbon source syntrophism and secondary metabolite induction. Appl Microbiol Biotechnol 103(1):411–425.  https://doi.org/10.1007/s00253-018-9469-4 CrossRefPubMedGoogle Scholar
  23. Hyun M, Kim J, Dumur C, Schroeder FC, You YJ (2016) BLIMP-1/BLMP-1 and metastasis-associated protein regulate stress resistant development in Caenorhabditis elegans. Genetics 203(4):1721–1732.  https://doi.org/10.1534/genetics.116.190793 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Janusz G, Kucharzyk KH, Pawlik A, Staszczak M, Paszczynski AJ (2013) Fungal laccase, manganese peroxidase and lignin peroxidase: gene expression and regulation. Enzym Microb Technol 52(1):1–12.  https://doi.org/10.1016/j.enzmictec.2012.10.003 CrossRefGoogle Scholar
  25. Kang G, Li G, Ma H, Wang C, Guo T (2013) Proteomic analysis on the leaves of TaBTF3 gene virus-induced silenced wheat plants may reveal its regulatory mechanism. J Proteome 83:130–143.  https://doi.org/10.1016/j.jprot.2013.03.020 CrossRefGoogle Scholar
  26. Kües U, Rühl M (2011) Multiple multi-copper oxidase gene families in basidiomycetes – What for? Current Genomics 12(2):72–94.  https://doi.org/10.2174/138920211795564377 CrossRefPubMedPubMedCentralGoogle Scholar
  27. Kuramoto N, Goto E, Masamune Y, Gion K, Yoneda Y (2002) Existence of xenobiotic response element binding in Dictyostelium. Biochim Biophys Acta 1578(1-3):1–11.  https://doi.org/10.1016/S0167-4781(02)00449-9 CrossRefPubMedGoogle Scholar
  28. Li B, Dewey CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinforma 12(1):323–323.  https://doi.org/10.1186/1471-2105-12-323 CrossRefGoogle Scholar
  29. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-Delta Delta C) method. Methods 25(4):402–408.  https://doi.org/10.1006/meth.2001.1262 CrossRefPubMedGoogle Scholar
  30. Luo F, Zhong Z, Liu L, Igarashi Y, Xie D, Li N (2017) Metabolomic differential analysis of interspecific interactions among white rot fungi Trametes versicolor, Dichomitus squalens and Pleurotus ostreatus. Sci Rep 7(1):5265.  https://doi.org/10.1038/s41598-017-05669-3 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Lv Y, Chen Y, Sun S, Hu Y (2014) Interaction among multiple microorganisms and effects of nitrogen and carbon supplementations on lignin degradation. Bioresour Technol 155:144–151.  https://doi.org/10.1016/j.biortech.2013.12.012 CrossRefPubMedGoogle Scholar
  32. Morin E, Kohler A, Baker AR, Foulongne-Oriol M, Lombard V, Nagy LG, Ohm RA, Patyshakuliyeva A, Brun A, Aerts AL, Bailey AM, Billette C, Coutinho PM, Deakin G, Doddapaneni H, Floudas D, Grimwood J, Hilden K, Kües U, Labutti KM, Lapidus A, Lindquist EA, Lucas SM, Murat C, Riley RW, Salamov AA, Schmutz J, Subramanian V, Wösten HA, Xu J, Eastwood DC, Foster GD, Sonnenberg AS, Cullen D, de Vries RP, Lundell T, Hibbett DS, Henrissat B, Burton KS, Kerrigan RW, Challen MP, Grigoriev IV, Martin F (2012) Genome sequence of the button mushroom Agaricus bisporus reveals mechanisms governing adaptation to a humic-rich ecological niche. Proc Natl Acad Sci U S A 109(43):17501–17506.  https://doi.org/10.1073/pnas.1206847109 CrossRefPubMedPubMedCentralGoogle Scholar
  33. Niu W, Lu ZJ, Zhong M, Sarov M, Murray JI, Brdlik CM, Janette J, Chen C, Alves P, Preston E, Slightham C, Jiang L, Hyman AA, Kim SK, Waterston RH, Gerstein M, Snyder M, Reinke V (2011) Diverse transcription factor binding features revealed by genome-wide ChIP-seq in C. elegans. Genome Res 21(2):245–254.  https://doi.org/10.1101/gr.114587.110 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Piscitelli A, Giardina P, Lettera V, Pezzella C, Sannia G, Faraco V (2011) Induction and transcriptional regulation of laccases in fungi. Current Genomics 12(2):104–112.  https://doi.org/10.2174/138920211795564331 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Pollegioni L, Tonin F, Rosini E (2015) Lignin-degrading enzymes. FEBS J 282(7):1190–1213.  https://doi.org/10.1111/febs.13224 CrossRefPubMedGoogle Scholar
  36. Qi-He C, Krugener S, Hirth T, Rupp S, Zibek S (2011) Co-cultured production of lignin-modifying enzymes with white-rot fungi. Appl Biochem Biotechnol 165(2):700–718.  https://doi.org/10.1007/s12010-011-9289-9 CrossRefPubMedGoogle Scholar
  37. Ramírez DFG, Vázquez RR, Pérez PA, Bustillos LGT, López RA, Horcasitas MCM, García FJE (2018) Crude enzymatic extract from Trametes maxima and Paecilomyces carneus mixed culture entrapped on alginate for phenanthrene removal in water. Environ Eng Sci 35(10):1126–1135.  https://doi.org/10.1089/ees.2018.0064 CrossRefGoogle Scholar
  38. Rivas-San Vicente M, Plasencia J (2011) Salicylic acid beyond defence: its role in plant growth and development. J Exp Bot 62(10):3321–3338.  https://doi.org/10.1093/jxb/err031 CrossRefPubMedGoogle Scholar
  39. Rivera-Hoyos CM, Morales-Alvarez ED, Poveda-Cuevas SA, Reyes-Guzman EA, Poutou-Pinales RA, Reyes-Montano EA, Pedroza-Rodriguez AM, Rodriguez-Vazquez R, Cardozo-Bernal AM (2015) Computational analysis and low-scale constitutive expression of laccases synthetic genes GlLCC1 from Ganoderma lucidum and POXA 1B from Pleurotus ostreatus in Pichia pastoris. PLoS One 10(1):e0116524.  https://doi.org/10.1371/journal.pone.0116524 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26(1):139–140.  https://doi.org/10.1093/bioinformatics/btp616 CrossRefGoogle Scholar
  41. Schroeckh V, Scherlach K, Nützmann H, Shelest E, Schmidt-Heck W, Schuemann J, Martin K, Hertweck C, Brakhage AA (2009) Intimate bacterial–fungal interaction triggers biosynthesis of archetypal polyketides in Aspergillus nidulans. Proc Natl Acad Sci USA 106(34):14558–14563.  https://doi.org/10.1073/pnas.0901870106 CrossRefPubMedGoogle Scholar
  42. Sharma A, Jain KK, Jain A, Kidwai M, Kuhad RC (2018) Bifunctional in vivo role of laccase exploited in multiple biotechnological applications. Appl Microbiol Biotechnol 102(24):10327–10343.  https://doi.org/10.1007/s00253-018-9404-8 CrossRefPubMedGoogle Scholar
  43. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28(5):511–515.  https://doi.org/10.1038/nbt.1621 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Wang H, Yu G, Li P, Gu Y, Li J, Liu G, Yao J (2009) Overproduction of Trametes versicolor laccase by making glucose starvation using yeast. Enzym Microb Technol 45(2):146–149.  https://doi.org/10.1016/j.enzmictec.2009.04.003 CrossRefGoogle Scholar
  45. Wang HJ, Liang R, Fu LM, Han RM, Zhang JP, Skibsted LH (2014) Nutritional aspects of beta-carotene and resveratrol antioxidant synergism in giant unilamellar vesicles. Food Funct 5(7):1573–1578.  https://doi.org/10.1039/c4fo00225c CrossRefPubMedGoogle Scholar
  46. Wang H, Peng L, Ding Z, Wu J, Shi G (2015) Stimulated laccase production of Pleurotus ferulae JM301 fungus by Rhodotorula mucilaginosa yeast in co-culture. Process Biochem 50(6):901–905.  https://doi.org/10.1016/j.procbio.2015.03.004 CrossRefGoogle Scholar
  47. Wang L, Gao W, Wu X, Zhao M, Qu J, Huang C, Zhang J (2018) Genome-wide characterization and expression analyses of Pleurotus ostreatus MYB transcription factors during developmental stages and under heat stress based on de novo sequenced genome. Int J Mol Sci 19(7):2052.  https://doi.org/10.3390/ijms19072052 CrossRefPubMedCentralGoogle Scholar
  48. Wei F, Hong Y, Liu J, Yuan J, Fang W, Peng H, Xiao Y (2010) Gongronella sp. induces overproduction of laccase in Panus rudis. J Basic Microbiol 50(1):98–103.  https://doi.org/10.1002/jobm.200900155 CrossRefPubMedGoogle Scholar
  49. Xiang Y, Karaveg K, Moremen KW (2016) Substrate recognition and catalysis by GH47 alpha-mannosidases involved in Asn-linked glycan maturation in the mammalian secretory pathway. Proc Natl Acad Sci U S A 113(49):E7890–E7899.  https://doi.org/10.1073/pnas.1611213113 CrossRefPubMedPubMedCentralGoogle Scholar
  50. Xiao YZ, Hong YZ, Li JF, Hang J, Tong PG, Fang W, Zhou CZ (2006) Cloning of novel laccase isozyme genes from Trametes sp. AH28-2 and analyses of their differential expression. Appl Microbiol Biotechnol 71(4):493–501.  https://doi.org/10.1007/s00253-005-0188-2 CrossRefPubMedGoogle Scholar
  51. Yang J, Fong HT, Xie Z, Tan JW, Inoue T (2015) Direct and positive regulation of Caenorhabditis elegans bed-3 by PRDM1/BLIMP1 ortholog BLMP-1. Biochim Biophys Acta 1849(9):1229–1236.  https://doi.org/10.1016/j.bbagrm.2015.07.012 CrossRefPubMedGoogle Scholar
  52. Yang L, Zheng C, Chen Y, Ying H (2018) FLO genes family and transcription factor MIG1 regulate Saccharomyces cerevisiae biofilm formation during immobilized fermentation. Front Microbiol 9:1860.  https://doi.org/10.3389/fmicb.2018.01860 CrossRefPubMedPubMedCentralGoogle Scholar
  53. Zengler K, Zaramela LS (2018) The social network of microorganisms - how auxotrophies shape complex communities. Nat Rev Microbiol 16(6):383–390.  https://doi.org/10.1038/s41579-018-0004-5 CrossRefPubMedPubMedCentralGoogle Scholar
  54. Zhong Z, Li L, Chang P, Xie H, Zhang H, Igarashi Y, Li N, Luo F (2017) Differential gene expression profiling analysis in Pleurotus ostreatus during interspecific antagonistic interactions with Dichomitus squalens and Trametes versicolor. Fungal Biol 121(12):1025–1036.  https://doi.org/10.1016/j.funbio.2017.08.008 CrossRefPubMedGoogle Scholar
  55. Zhong Z, Li L, He B, Igarashi Y, Luo F (2019) Transcriptome analysis of differential gene expression in Dichomitus squalens during interspecific mycelial interactions and the potential link with laccase induction. J Microbiol 57(2):127–137.  https://doi.org/10.1007/s12275-019-8398-y CrossRefPubMedGoogle Scholar
  56. Zhou L, Ouyang L, Lin S, Chen S, Liu Y, Zhou W, Wang X (2018) Protective role of beta-carotene against oxidative stress and neuroinflammation in a rat model of spinal cord injury. Int Immunopharmacol 61:92–99.  https://doi.org/10.1016/j.intimp.2018.05.022 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Qi Zhang
    • 1
    • 2
  • Liting Zhao
    • 2
  • YouRan Li
    • 1
    • 2
  • Feng Wang
    • 3
  • Song Li
    • 4
  • Guiyang Shi
    • 1
    • 2
  • Zhongyang Ding
    • 1
    • 2
    Email author
  1. 1.Key Laboratory of Carbohydrate Chemistry and Biotechnology, Ministry of Education, School of BiotechnologyJiangnan UniversityWuxiChina
  2. 2.National Engineering Laboratory for Cereal Fermentation TechnologyJiangnan UniversityWuxiChina
  3. 3.School of Food and Biological EngineeringJiangsu UniversityZhenjiangChina
  4. 4.School of Biological and Chemical EngineeringAnhui Polytechnic UniversityWuhuChina

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