Abstract
Distinct wood degraders occupying their preferred habitats have biased enzyme repertoires that are well fitted to their colonized substrates. Pleurotus ostreatus, commonly found on wood, has evolved its own enzyme-producing traits. In our previous study, transcriptional shifts in several P. ostreatus delignification-defective mutants, including Δhir1 and Δgat1 strains, were analyzed, which revealed the downregulation of ligninolytic genes and the upregulation of cellulolytic and xylanolytic genes when compared to their parental strain 20b on beech wood sawdust medium (BWS). In this study, rice straw (RS) was used as an alternative substrate to examine the transcriptional responses of P. ostreatus to distinct substrates. The vp1 gene and a cupredoxin-encoding gene were significantly upregulated in the 20b strain on RS compared with that on BWS, reflecting their distinct regulation patterns. The overall expression level of genes encoding glucuronidases was also higher on RS than on BWS, showing a good correlation with the substrate composition. Transcriptional alterations in the mutants (Δhir1 or Δgat1 versus 20b strain) on RS were similar to those on BWS, and the extracellular lignocellulose-degrading enzyme activities and lignin-degrading ability of the mutants on RS were consistent with the transcriptional alterations of the corresponding enzyme-encoding genes. However, transcripts of specific genes encoding enzymes belonging to the same CAZyme family exhibited distinct alteration patterns in the mutant strains grown on RS compared to those grown on BWS. These findings provide new insights into the molecular mechanisms underlying the transcriptional regulation of lignocellulolytic genes in P. ostreatus.
Key Points
• P. ostreatus expressed variable enzymatic repertoire-related genes in response to distinct substrates.
• A demand to upregulate the cellulolytic genes seems to be present in ligninolysis-deficient mutants.
• The regulation of some specific genes probably driven by the demand is dependent on the substrate.
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Data availability
All data supporting the claims of this manuscript are presented and made available in this manuscript.
References
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 18:4710–4726. https://doi.org/10.1111/1462-2920.13360
Alfaro M, Majcherczyk A, Kües U, Ramírez L, Pisabarro AG (2020) Glucose counteracts wood-dependent induction of lignocellulolytic enzyme secretion in monokaryon and dikaryon submerged cultures of the white-rot basidiomycete Pleurotus ostreatus. Sci Rep 10:12421. https://doi.org/10.1038/s41598-020-68969-1
Álvarez JM, Canessa P, Mancilla RA, Polanco R, Santibáñez PA, Vicuña R (2009) Expression of genes encoding laccase and manganese-dependent peroxidase in the fungus Ceriporiopsis subvermispora is mediated by an ACE1-like copper-fist transcription factor. Fungal Genet Biol 46:104–111. https://doi.org/10.1016/j.fgb.2008.10.002
Antoniêto ACC, dos Santos CL, Silva-Rocha R, Persinoti GF, Silva RN (2014) Defining the genome-wide role of CRE1 during carbon catabolite repression in Trichoderma reesei using RNA-Seq analysis. Fungal Genet Biol 73:93–103. https://doi.org/10.1016/j.fgb.2014.10.009
Ashraf J, Ali MA, Ahmad W, Ayyub CM, Shafi J (2013) Effect of different substrate supplements on oyster mushroom (Pleurotus spp) production. Food Sci Technol 1:44–51. https://doi.org/10.13189/fst.2013.010302
Bailey TL, Elkan C (1994) Fitting a mixture model by expectation maximization to discover motifs in bipolymers. Proc Int Conf Intell Syst Mol Biol 2:28–36
Bayry J, Aimanianda V, Guijarro JI, Sunde M, Latge JP (2012) Hydrophobins—unique fungal proteins. PLoS Pathog 8(5):e1002700. https://doi.org/10.1371/journal.ppat.1002700
Billa E, Monties B (1995) Molecular variability of lignin fractions isolated from wheat straw. Res Chem Intermed 21(3-5):303–311. https://doi.org/10.1007/BF03052260
Boraston AB, Bolam DN, Gilbert HJ, Davies GJ (2004) Carbohydrate-binding modules: fine-tuning polysaccharide recognition. Biochem J 382:769–781. https://doi.org/10.1042/BJ20040892
Brown NA, Ries LN, Reis TF, Rajendran R, Dos Santos RAC, Ramage G, Riaño-Pachón DM, Goldman GH (2016) RNA-seq reveals hydrophobins that are involved in the adaptation of Aspergillus nidulans to lignocellulose. Biotechnol Biofuels 9:p145. https://doi.org/10.1186/s13068-016-0558-2
Campbell JA, Davies GJ, Bulone V, Henrissat B (1997) A classification of nucleotide-diphospho-sugar glycosyltransferases based on amino acid sequence similarities. Biochem J 326:929–939. https://doi.org/10.1042/bj3260929u
Delmas S, Pullan ST, Gaddipati S, Kokolski M, Malla S, Blythe MJ, Ibbett R, Campbell M, Liddell S, Aboobaker A, Tucker GA, Archer DB (2012) Uncovering the genome-wide transcriptional responses of the filamentous fungus Aspergillus niger to lignocellulose using RNA sequencing. PLoS Genet 8:e1002875. https://doi.org/10.1371/journal.pgen.1002875
Deng W, Wang Y, Liu Z, Cheng H, Xue Y (2014) HemI: a toolkit for illustrating heatmaps. PLoS One 9:e111988. https://doi.org/10.1371/journal.pone.0111988
Dodds PN, Rafiqi M, Gan PH, Hardham AR, Jones DA, Ellis JG (2009) Effectors of biotrophic fungi and oomycetes: pathogenicity factors and triggers of host resistance. New Phytol 183:993–1000. https://doi.org/10.1111/j.1469-8137.2009.02922.x
Feldman D, Kowbel DJ, Glass NL, Yarden O, Hadar Y (2017) A role for small secreted proteins (SSPs) in a saprophytic fungal lifestyle: ligninolytic enzyme regulation in Pleurotus ostreatus. Sci Rep 7:1–13. https://doi.org/10.1038/s41598-017-15112-2
Fernández-Fueyo E, Castanera R, Ruiz-Dueñas FJ, López-Lucendo MF, Ramírez L, Pisabarro AG, Martínez AT (2014) Ligninolytic peroxidase gene expression by Pleurotus ostreatus: differential regulation in lignocellulose medium and effect of temperature and pH. Fungal Genet Biol 72:150–161. https://doi.org/10.1016/j.fgb.2014.02.003
Fernández-Fueyo E, Ruiz-Dueñas FJ, López-Lucendo MF, Pérez-Boada M, Rencoret J, Gutiérrez A, Pisabarro AG, Ramírez L, Martínez AT (2016) A secretomic view of woody and nonwoody lignocellulose degradation by Pleurotus ostreatus. Biotechnol Biofuels 9:49. https://doi.org/10.1186/s13068-016-0462-9
Floudas D, Binder M, Riley R, Barry K, Blanchette RA, Henrissat B, Martinez AT, Otillar R, Spatafora JW, Yadav JS, Aerts A, Benoit I, Boyd A, Carlson A, Copeland A, Coutinho PM, de Vries RP, Ferreira P, Findley K, Foster B, Gaskell J, Glotzer D, Gorecki P, Heitman J, Hesse C, Hori C, Igarashi K, Jurgens JA, Kallen N, Kersten P, Kohler A, Kües U, Kumar TK, Kuo A, LaButti K, Larrondo LF, Lindquist E, Ling A, Lombard V, Lucas S, Lundell T, Martin R, McLaughlin DJ, Morgenstern I, Morin E, Murat C, Nagy LG, Nolan M, Ohm RA, Patyshakuliyeva A, Rokas A, Ruiz-Dueñas FJ, Sabat G, Salamov A, Samejima M, Schmutz J, Slot JC, John FS, Stenlid J, Sun H, Sun S, Syed K, Tsang A, Wiebenga A, Young D, Pisabarro A, Eastwood DC, Martin F, Cullen D, Grigoriev IV, Hibbett DS (2012) The Paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science 336:1715–1719. https://doi.org/10.1126/science.1221748
Gupta S, Stamatoyannopoulos JA, Bailey TL, Noble WS (2007) Quantifying similarity between motifs. Genome Biol 8:R24. https://doi.org/10.1186/gb-2007-8-2-r24
Henrissat B (1991) A classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem J 280:309–316. https://doi.org/10.1042/bj2800309
Hoa HT, Wang CL, Wang CH (2015) The effects of different substrates on the growth, yield, and nutritional composition of two oyster mushrooms (Pleurotus ostreatus and Pleurotus cystidiosus). Mycobiology 43:423–434. https://doi.org/10.5941/MYCO.2015.43.4.423
Hobert O (2008) Gene regulation by transcription factors and microRNAs. Science 319:1785–1786. https://doi.org/10.1126/science.1151651
Honda Y, Matsuyama T, Irie T, Watanabe T, Kuwahara M (2000) Carboxin resistance transformation of the homobasidiomycete fungus Pleurotus ostreatus. Curr Genet 37:209–212. https://doi.org/10.1007/s002940050521
Hori C, Gaskell J, Igarashi K, Kersten P, Mozuch M, Samejima M, Cullen D (2014) Temporal alterations in the secretome of the selective ligninolytic fungus Ceriporiopsis subvermispora during growth on aspen wood reveal this organism's strategy for degrading lignocellulose. Appl Environ Microbiol 80:2062–2070. https://doi.org/10.1128/AEM.03652-13
Jaenisch R, Bird A (2003) Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet 33:245–254. https://doi.org/10.1038/ng1089
Janusz G, Pawlik A, Sulej J, Świderska-Burek U, Jarosz-Wilkołazka A, Paszczyński A (2017) Lignin degradation: microorganisms, enzymes involved, genomes analysis and evolution. FEMS Microbiol Rev 41:941–962. https://doi.org/10.1093/femsre/fux049
Kamitsuji H, Honda Y, Watanabe T, Kuwahara M (2004) Production and induction of manganese peroxidase isozymes in a white-rot fungus Pleurotus ostreatus. Appl Microbiol Biotechnol 65:287–294. https://doi.org/10.1007/s00253-003-1543-9
Kersten P, Cullen D (2014) Copper radical oxidases and related extracellular oxidoreductases of wood-decay Agaricomycetes. Fungal Genet Biol 72:124–130. https://doi.org/10.1016/j.fgb.2014.05.011
Kim KT, Jeon J, Choi J, Cheong K, Song H, Choi G, Lee YH (2016) Kingdom-wide analysis of fungal small secreted proteins (SSPs) reveals their potential role in host association. Front Plant Sci 7:186. https://doi.org/10.3389/fpls.2016.00186
Knop D, Ben-Ari J, Salame TM, Levinson D, Yarden O, Hadar Y (2014) Mn2+-deficiency reveals a key role for the Pleurotus ostreatus versatile peroxidase (VP4) in oxidation of aromatic compounds. Appl Microbiol Biotechnol 98:6795–6804. https://doi.org/10.1007/s00253-014-5689-4
König J, Grasser R, Pikor H, Vogel K (2002) Determination of xylanase, β-glucanase, and cellulase activity. Anal Bioanal Chem 374:80–87. https://doi.org/10.1007/s00216-002-1379-7
Kormelink FJM, Voragen AGJ (1993) Degradation of different [(glucurono) arabino] xylans by a combination of purified xylan-degrading enzymes. Appl Microbiol Biotechnol 38:688–695. https://doi.org/10.1007/BF00182811
Kotake T, Kawamoto H, Saka S (2015) Pyrolytic formation of monomers from hardwood lignin as studied from the reactivities of the primary products. J Anal Appl Pyrolysis 113:57–64. https://doi.org/10.1016/j.jaap.2014.09.029
Koutaniemi S, van Gool MP, Juvonen M, Jokela J, Hinz SW, Schols HA, Tenkanen M (2013) Distinct roles of carbohydrate esterase family CE16 acetyl esterases and polymer-acting acetyl xylan esterases in xylan deacetylation. J Biotechnol 168:684–692. https://doi.org/10.1016/j.jbiotec.2013.10.009
Kracher D, Scheiblbrandner S, Felice AK, Breslmayr E, Preims M, Ludwicka K, Haltrich D, Eijsink VG, Ludwig R (2016) Extracellular electron transfer systems fuel cellulose oxidative degradation. Science 352:1098–1101. https://doi.org/10.1126/science.aaf3165
Levasseur A, Drula E, Lombard V, Coutinho PM, Henrissat B (2013) Expansion of the enzymatic repertoire of the CAZy database to integrate auxiliary redox enzymes. Biotechnol Biofuels 6:41. https://doi.org/10.1186/1754-6834-6-41
Lombard V, Bernard T, Rancurel C, Brumer H, Coutinho PM, Henrissat B (2010) A hierarchical classification of polysaccharide lyases for glycogenomics. Biochem J 432:437–444. https://doi.org/10.1042/BJ20101185
Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B (2013) The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res 42:D490–D495. https://doi.org/10.1093/nar/gkt1178
Lundell TK, Mäkelä MR, Hildén K (2010) Lignin-modifying enzymes in filamentous basidiomycetes-ecological, functional and phylogenetic review. J Basic Microbiol 50:5–20. https://doi.org/10.1002/jobm.200900338
Manavalan T, Manavalan A, Heese K (2015) Characterization of lignocellulolytic enzymes from white-rot fungi. Curr Microbiol 70:485–498. https://doi.org/10.1007/s00284-014-0743-0
Mueller-Harvey I, Hartley RD, Harris PJ, Curzon EH (1986) Linkage of p-coumaroyl and feruloyl groups to cell-wall polysaccharides of barley straw. Carbohydr Res 148:71–85. https://doi.org/10.1016/0008-6215(86)80038-6
Nagy LG, Merényi Z, Hegedüs B, Bálint B (2020) Novel phylogenetic methods are needed for understanding gene function in the era of mega-scale genome sequencing. Nucleic Acids Res 48:2209–2219. https://doi.org/10.1093/nar/gkz1241
Nakazawa T, Tsuzuki M, Irie T, Sakamoto M, Honda Y (2016) Marker recycling via 5-fluoroorotic acid and 5-fluorocytosine counter-selection in the white-rot agaricomycete Pleurotus ostreatus. Fungal Biol 120:1146–1155. https://doi.org/10.1016/j.funbio.2016.06.011
Nakazawa T, Izuno A, Kodera R, Miyazaki Y, Sakamoto M, Isagi Y, Honda Y (2017a) Identification of two mutations that cause defects in the ligninolytic system through efficient forward genetics in the white-rot agaricomycete Pleurotus ostreatus. Environ Microbiol 19:261–272. https://doi.org/10.1111/1462-2920.13595
Nakazawa T, Izuno A, Horii M, Kodera R, Nishimura H, Hirayama Y, Tsunematsu Y, Miyazaki Y, Awano T, Muraguchi H, Watanabe K, Sakamoto M, Takabe K, Watanabe T, Isagi Y, Honda Y (2017b) Effects of pex1 disruption on wood lignin biodegradation, fruiting development and the utilization of carbon sources in the white-rot Agaricomycete Pleurotus ostreatus and non-wood decaying Coprinopsis cinerea. Fungal Genet Biol 109:7–15. https://doi.org/10.1016/j.fgb.2017.10.002
Nakazawa T, Morimoto R, Wu H, Kodera R, Sakamoto M, Honda Y (2019) Dominant effects of gat1 mutations on the ligninolytic activity of the white-rot fungus Pleurotus ostreatus Fungal. Biol 123:209–217. https://doi.org/10.1016/j.funbio.2018.12.007
Peddireddi S, Velagapudi R, Hoegger PJ, Majcherczyk A, Naumann A, Polle A, Kües U (2006) Multiple hydrophobin genes in mushrooms In Pisabarro AG, Ramírez L (eds): VI Meeting on Genetics and Cellular Biology of Basidiomycetes (GCBB-VI) Pamplona: Universidad Pública de Navarra/Nafarroako Unibertsitate Publikoa, pp 151-163
Pellegrin C, Morin E, Martin FM, Veneault-Fourrey C (2015) Comparative analysis of secretomes from ectomycorrhizal fungi with an emphasis on small-secreted proteins. Front Microbiol 6:1278. https://doi.org/10.3389/fmicb.2015.01278
Peñas MM, Rust B, Larraya LM, Ramírez L, Pisabarro AG (2002) Differentially regulated, vegetative-mycelium-specific hydrophobins of the edible basidiomycete Pleurotus ostreatus. Appl Environ Microbiol 68:3891–3898. https://doi.org/10.1128/AEM.68.8.3891-3898.2002
Petrini O, Sieber TN, Toti L, Viret O (1993) Ecology, metabolite production, and substrate utilization in endophytic fungi. Nat Toxins 1:185–196. https://doi.org/10.1002/nt.2620010306
Plett JM, Kemppainen M, Kale SD, Kohler A, Legué V, Brun A, Martin F (2011) A secreted effector protein of Laccaria bicolor is required for symbiosis development. Curr Biol 21:1197–1203. https://doi.org/10.1016/j.cub.2011.05.033
Rao PS, Niederpruem DJ (1969) Carbohydrate metabolism during morphogenesis of Coprinus lagopus (sensu Buller). J Bacteriol 100:1222–1228
Ritter GJ, Seborg RM, Mitchell RL (1932) Factors affecting quantitative determination of lignin by 72 per cent sulfuric acid method. Ind Eng Chem Anal Ed 4:202–204
Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139–140. https://doi.org/10.1093/bioinformatics/btp616
Rytioja J, Hildén K, Yuzon J, Hatakka A, de Vries RP, Mäkelä MR (2014) Plant-polysaccharide-degrading enzymes from basidiomycetes. Microbiol Mol Biol Rev 78:614–649. https://doi.org/10.1128/MMBR.00035-14
Rytioja J, Hildén K, Di Falco M, Zhou M, Aguilar-Pontes MV, Sietiö OM, Tsang A, de Vries RP, Mäkelä MR (2017) The molecular response of the white-rot fungus Dichomitus squalens to wood and non-woody biomass as examined by transcriptome and exoproteome analyses. Environ Microbiol 19:1237–1250. https://doi.org/10.1111/1462-2920.13652
Salame TM, Knop D, Tal D, Levinson D, Yarden O, Hadar Y (2012) Predominance of a versatile-peroxidase-encoding gene, mnp4, as demonstrated by gene replacement via a gene targeting system for Pleurotus ostreatus. Appl Environ Microbiol 78:5341–5352. https://doi.org/10.1128/AEM.01234-12
Salame TM, Knop D, Levinson D, Mabjeesh SJ, Yarden O, Hadar Y (2014) Inactivation of a Pleurotus ostreatus versatile peroxidase-encoding gene (mnp2) results in reduced lignin degradation. Environ Microbiol 16:265–277. https://doi.org/10.1111/1462-2920.12279
Saloheimo M, Paloheimo M, Hakola S, Pere J, Swanson B, Nyyssönen E, Penttilä M (2002) Swollenin, a Trichoderma reesei protein with sequence similarity to the plant expansins, exhibits disruption activity on cellulosic materials. Eur J Biochem 269:4202–4211. https://doi.org/10.1046/j.1432-1033.2002.03095.x
Semenova TA, Dunaevsky YE, Beljakova GA, Borisov BA, Shamraichuk IL, Belozersky MA (2017) Extracellular peptidases as possible markers of fungal ecology. Appl Soil Ecol 113:1–10. https://doi.org/10.1016/j.apsoil.2017.01.002
Shibuya N, Iwasaki T (1985) Structural features of rice bran hemicellulose. Phytochemistry 24:285–289. https://doi.org/10.1016/S0031-9422(00)83538-4
Sjostrom E (1993) Wood chemistry: fundamentals and applications Gulf professional publishing. Academic Press, San Diego. https://doi.org/10.1016/B978-0-08-092589-9.50005-X
Sun RC, Sun XF, Zhang SH (2001) Quantitative determination of hydroxycinnamic acids in wheat, rice, rye, and barley straws, maize stems, oil palm frond fiber, and fast-growing poplar wood. J Agric Food Chem 49:5122–5129. https://doi.org/10.1021/jf010500r
Sunna A, Antranikian G (1997) Xylanolytic enzymes from fungi and bacteria. Crit Rev Biotechnol 17:39–67. https://doi.org/10.3109/07388559709146606
Toyokawa C, Shobu M, Tsukamoto R, Okamura S, Honda Y, Kamitsuji H, Izumitsu K, Suzuki K, Irie T (2016) Effects of overexpression of PKAc genes on expressions of lignin-modifying enzymes by Pleurotus ostreatus. Biosci Biotechnol Biochem 80:1759–1767. https://doi.org/10.1080/09168451.2016.1158630
Tsukihara T, Honda Y, Sakai R, Watanabe T, Watanabe T (2006) Exclusive overproduction of recombinant versatile peroxidase MnP2 by genetically modified white rot fungus, Pleurotus ostreatus. J Biotechnol 126:431–439. https://doi.org/10.1016/j.jbiotec.2006.05.013
Tzfadia O, Diels T, De Meyer S, Vandepoele K, Aharoni A, Van de Peer Y (2016) CoExpNetViz: comparative co-expression networks construction and visualization tool. Front Plant Sci 6:1194. https://doi.org/10.3389/fpls.2015.01194
Vanholme R, Demedts B, Morreel K, Ralph J, Boerjan W (2010) Lignin biosynthesis and structure. Plant Physiol 153:895–905. https://doi.org/10.1104/pp.110.155119
Wösten HA (2001) Hydrophobins: multipurpose proteins. Annu Rev Microbiol 55:625–646. https://doi.org/10.1146/annurev.micro.55.1.625
Wu B, Gaskell J, Zhang J, Toapanta C, Ahrendt S, Grigoriev IV, Blanchette RA, Schilling JS, Master E, Cullen D, Hibbett DS (2019) Evolution of substrate-specific gene expression and RNA editing in brown rot wood-decaying fungi. ISME J 13:1391–1403. https://doi.org/10.1038/s41396-019-0359-2
Wu H, Nakazawa T, Takenaka A, Kodera R, Morimoto R, Sakamoto M, Honda Y (2020) Transcriptional shifts in delignification-defective mutants of the white-rot fungus Pleurotus ostreatus. FEBS Lett 594:3182–3199. https://doi.org/10.1002/1873-3468.13890
Wu H, Nakazawa T, Morimoto R, Shivani, Sakamoto M, Honda Y (2021) Targeted disruption of hir1 alters the transcriptional expression pattern of putative lignocellulolytic genes in the white-rot fungus Pleurotus ostreatus. Fungal Genet Biol 147:103507. https://doi.org/10.1016/j.fgb.2020.103507
Xiao B, Sun X, Sun R (2001) Chemical, structural, and thermal characterizations of alkali-soluble lignins and hemicelluloses, and cellulose from maize stems, rye straw, and rice straw. Polym Degrad Stab 74:307–319. https://doi.org/10.1016/S0141-3910(01)00163-X
Yoav S, Salame TM, Feldman D, Levinson D, Ioelovich M, Morag E, Yarden O, Bayer EA, Hadar Y (2018) Effects of cre1 modification in the white-rot fungus Pleurotus ostreatus PC9: altering substrate preference during biological pretreatment. Biotechnol Biofuels 11:212. https://doi.org/10.1186/s13068-018-1209-6
Zoghlami A, Paës G (2019) Lignocellulosic biomass: understanding recalcitrance and predicting hydrolysis. Front Chem 7:874. https://doi.org/10.3389/fchem.2019.00874
Zong Z, He R, Fu H, Zhao T, Chen S, Shao X, Zhang D, Cai W (2016) Pretreating cellulases with hydrophobins for improving bioconversion of cellulose: an experimental and computational study. Green Chem 18:6666–6674. https://doi.org/10.1039/C6GC02694J
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We would like to thank Prof. Yitzhak Hadar (Hebrew University of Jerusalem, Israel) for providing P. ostreatus strain 20b.
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This work was supported in part by the Institute for Fermentation, Osaka [to T.N.], JSPS KAKENHIs [16K18729 and 19H03017 to T.N.], and the China Scholarship Council [to H.W.].
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TN conceived and designed the study. HLW carried out the experiment and drafted the manuscript. HLW, HBX, RHY, DPB and MK performed the analyses, TN, MK, MS, and YH provided editorial suggestions and revisions. All authors read and approved the final manuscript.
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Wu, H., Nakazawa, T., Xu, H. et al. Comparative transcriptional analyses of Pleurotus ostreatus mutants on beech wood and rice straw shed light on substrate-biased gene regulation. Appl Microbiol Biotechnol 105, 1175–1190 (2021). https://doi.org/10.1007/s00253-020-11087-9
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DOI: https://doi.org/10.1007/s00253-020-11087-9