Tailoring in fungi for next generation cellulase production with special reference to CRISPR/CAS system

Abstract

Cellulose is the utmost plenteous source of biopolymer in our earth, and fungi are the most efficient and ubiquitous organism in degrading the cellulosic biomass by synthesizing cellulases. Tailoring through genetic manipulation has played a substantial role in constructing novel fungal strains towards improved cellulase production of desired traits. However, the traditional methods of genetic manipulation of fungi are time-consuming and tedious. With the availability of the full-genome sequences of several industrially relevant filamentous fungi, CRISPR-CAS (clustered regularly interspaced short palindromic repeats/CRISPR-associated protein) technology has come into the focus for the proficient development of manipulated strains of filamentous fungi. This review summarizes the mode of action of cellulases, transcription level regulation for cellulase expression, various traditional strategies of genetic manipulation with CRISPR-CAS technology to develop modified fungal strains for a preferred level of cellulase production, and the futuristic trend in this arena of research.

Keywords

Cellulose / Cellulase / Fungi / Genetic manipulation / CRISPR / CAS / Biological Sciences / Genetics

References

[1] BaruahJ, NathBK, SharmaR, KumarS, DekaRC, BaruahDC, KalitaE. Recent trends in the pretreatment of lignocellulosic biomass for value-added products. Front Energy Res, 2018, 186141

[2] DasA, PaulT, HalderSK, Das MohapatraPK, PatiBR, MondalKC. Study on regulation of growth and biosynthesis of cellulolytic enzymes from newly isolated Aspergillus fumigatus ABK9. Pol J Microbiol, 2013, 62131-43

[3] DasA, PaulT, HalderSK, JanaA, GhoshK, MaityC, Das MohapatraPK, PatiBR, MondalKC. Low cost single-step purification of endoglucanase from Aspergillus fumigates ABK9. Ind J Exp Biol, 2013, 5111954-959

[4] ParkS, BakerJO, HimmelME, ParillaPA, JohnsonDK. Cellulose crystallinity index: measurement techniques and their impact on interpreting cellulase performance. Biotechnol Biofuels, 2010, 311

[5] WangBT, HuS, YuXY, JinL, ZhuYJ, JinFJ. Studies of cellulose and starch utilization and the regulatory mechanisms of related enzymes in fungi. Polymers, 2020, 123530

[6] MondalS, HalderSK, MondalKCYadavAN, SinghS, MishraS, GuptaA. Fungal enzymes for bioconversion of lignocellulosic biomass. Recent advancement in white biotechnology through fungi, 2019ChamSpringer349-380

[7] DasA, JanaA, PaulT, HalderSK, GhoshK, MaityC, Das MohapatraPK, PatiBR, MondalKC. Thermodynamics and kinetic properties of halostable endoglucanase from Aspergillus fumigatus ABK9. J Basic Microbiol, 2014, 54: S142-S151

[8] MondalS, SorenJP, MondalJ, RakshitS, HalderSK, MondalKC. Contemporaneous synthesis of multiple carbohydrate debranching enzymes from newly isolated Aspergillus fumigatus SKF-2 under solid state fermentation: a unique enzyme mixture for proficient saccharification of plant bioresources. Ind Crops Prod, 2020, 150112409

[9] ZhaoXQ, ZhangXY, ZhangF, ZhangR, JiangBJ, BaiFWXuF, QuY. Metabolic engineering of fungal strains for efficient production of cellulolytic enzymes. Fungal cellulolytic enzymes, 2018SingaporeSpringer27-41

[10] DasA, PaulT, HalderSK, JanaA, MaityC, Das MohapatraPK, PatiBR, MondalKC. Production of cellulolytic enzymes by Aspergillus fumigatus ABK9 in wheat bran-rice straw mixed substrate and use of cocktail enzymes for deinking of waste office paper pulp. Bioresour Technol, 2013, 128: 290-296

[11] ChandelAK, RudravaramR, RaoLV, RavindraP, NarasuML. Industrial enzymes in bioindustrial sector development: an Indian perspective. J Commer Biotechnol, 2007, 134283-291

[12] JayasekaraS, RatnayakeR. Microbial cellulases: an overview and applications. Cellulose, 2019.

[13] de FrançaPD, PereiraNJr, de CastroAM. A comparative review of recent advances in cellulases production by Aspergillus, Penicillium and Trichoderma strains and their use for lignocellulose deconstruction. Curr Opin Green Sustain Chem, 2018, 14: 60-66

[14] AdebamiGE, Adebayo-TayoBCKuilaA, SharmaV. Development of cellulolytic strain by genetic engineering approach for enhanced cellulase production. Genetic and metabolic engineering for improved biofuel production from lignocellulosic biomass, 20201Elsevier103-136

[15] McCartyNS, GrahamAE, StudenáL, Ledesma-AmaroR. Multiplexed CRISPR technologies for gene editing and transcriptional regulation. Nat Commun, 2020, 1111-13

[16] SukumaranRK, ChristopherM, Kooloth-ValappilP, Sreeja-RajuA, MathewRM, SankarM, PuthiyamadamA, AdarshVP, AswathiA, RebinroV, AbrahamA. Addressing challenges in production of cellulases for biomass hydrolysis: targeted interventions into the genetics of cellulase producing fungi. Bioresour Technol, 2021, 329124746

[17] PatelAK, SinghaniaRR, SimSJ, PandeyA. Thermostable cellulases: current status and perspectives. Bioresour Technol, 2019, 279: 385-392

[18] SinghaniaRR, DixitP, PatelAK, GiriBS, KuoCH, ChenCW, Di DongC. Role and significance of lytic polysaccharide monooxygenases (LPMOs) in lignocellulose deconstruction. Bioresour Technol, 2021, 335125261

[19] MüllerG, ChylenskiP, BissaroB, EijsinkVG, HornSJ. The impact of hydrogen peroxide supply on LPMO activity and overall saccharification efficiency of a commercial cellulase cocktail. Biotechnol Biofuels, 2018, 1111-7

[20] ZhangF, BunterngsookB, LiJX, ZhaoXQ, ChampredaV, LiuCG, BaiFWLiY, GeX. Regulation and production of lignocellulolytic enzymes from Trichoderma reesei for biofuels production. Advances in bioenergy, 2019Elsevier79-1194

[21] BakerJO, KingMR, AdneyWS, DeckerSR, VinzantTB, LantzSE, NievesRE, ThomasSR, LiLC, CosgroveDJ, HimmelMEFinkelsteinM, DavisonBH. Investigation of the cell-wall loosening protein expansin as a possible additive in the enzymatic saccharification of lignocellulosic biomass. Twenty-first symposium on biotechnology for fuels and chemicals, 20001TotowaHumana Press217-223

[22] AndbergM, PenttiläM, SaloheimoM. Swollenin from Trichoderma reesei exhibits hydrolytic activity against cellulosic substrates with features of both endoglucanases and cellobiohydrolases. Bioresour Technol, 2015, 181: 105-113

[23] DruzhininaIS, KubicekCP. Genetic engineering of Trichoderma reesei cellulases and their production. Microb Biotechnol, 2017, 1061485-1499

[24] da Silva DelabonaP, RodriguesGN, ZubietaMP, RamoniJ, CodimaCA, LimaDJ, FarinasCS, da Cruz PradellaJG, SeibothB. The relation between xyr1 overexpression in Trichoderma harzianum and sugarcane bagasse saccharification performance. J Biotechnol, 2017, 246: 24-32

[25] DerntlC, Gudynaite-SavitchL, CalixteS, WhiteT, MachRL, Mach-AignerAR. Mutation of the xylanase regulator 1 causes a glucose blind hydrolase expressing phenotype in industrially used Trichoderma strains. Biotechnol Biofuels, 2013, 611-1

[26] ElliläS, FonsecaL, UchimaC, CotaJ, GoldmanGH, SaloheimoM, SaconV, Siika-AhoM. Development of a low-cost cellulase production process using Trichoderma reesei for Brazilian biorefineries. Biotechnol Biofuels, 2017, 1011-7

[27] RassingerA, Gacek-MatthewsA, StraussJ, MachRL, Mach-AignerAR. Truncation of the transcriptional repressor protein Cre1 in Trichoderma reesei Rut-C30 turns it into an activator. Fungal Biol Biotechnol, 2018, 511-8

[28] ZhangXY, ZiLH, GeXM, LiYH, LiuCG, BaiFW. Development of Trichoderma reesei mutants by combined mutagenesis and induction of cellulase by low-cost corn starch hydrolysate. Process Biochem, 2017, 54: 96-101

[29] WangS, LiuG, WangJ, YuJ, HuangB, XingM. Enhancing cellulase production in Trichoderma reesei RUT C30 through combined manipulation of activating and repressing genes. J Ind Microbiol Biotechnol, 2013, 406633-641

[30] WangS, LiuG, YuJ, TianS, HuangB, XingM. RNA interference with carbon catabolite repression in Trichoderma koningii for enhancing cellulase production. Enzyme Microb Technol, 2013, 532104-109

[31] ZhangF, ZhaoX, BaiF. Improvement of cellulase production in Trichoderma reesei Rut-C30 by overexpression of a novel regulatory gene Trvib-1. Bioresour Technol, 2018, 247: 676-683

[32] ZhangJ, WuC, WangW, WeiD. Construction of enhanced transcriptional activators for improving cellulase production in Trichoderma reesei RUT C30. Bioresour Bioprocess, 2018, 511-2

[33] XiongY, SunJ, GlassNL. VIB1, a link between glucose signaling and carbon catabolite repression, is essential for plant cell wall degradation by Neurospora crassa. PLoS Genet, 2014, 108e1004500

[34] ZhangJ, ZhangG, WangW, WeiD. Enhanced cellulase production in Trichoderma reesei RUT C30 via constitution of minimal transcriptional activators. Microb Cell Fact, 2018, 1711-4

[35] LiY, ZhangX, XiongL, MehmoodMA, ZhaoX, BaiF. On-site cellulase production and efficient saccharification of corn stover employing cbh2 overexpressing Trichoderma reesei with novel induction system. Bioresour Technol, 2017, 238: 643-649

[36] KiesenhoferDP, MachRL, Mach-AignerAR. Influence of cis element arrangement on promoter strength in Trichoderma reesei. Appl Environ Microbiol, 2018, 841e01742-17

[37] HirasawaH, ShioyaK, FurukawaT, TaniS, SumitaniJI, KawaguchiT, MorikawaY, ShidaY, OgasawaraW. Engineering of the Trichoderma reesei xylanase3 promoter for efficient enzyme expression. Appl Microbiol Biotechnol, 2018, 10262737-2752

[38] WangW, MengF, LiuP, YangS, WeiD. Construction of a promoter collection for genes co-expression in filamentous fungus Trichoderma reesei. J Ind Microbiol Biotechnol, 2014, 41111709-1718

[39] AlrikssonB, RoseSH, Van-ZylWH, SjödeA, NilvebrantNO, JönssonLJ. Cellulase production from spent lignocellulose hydrolysates by recombinant Aspergillus niger. Appl Environ Microbiol, 2009, 7582366-2374

[40] HongJ, TamakiH, YamamotoK, KumagaiH. Cloning of a gene encoding thermostable cellobiohydrolase from Thermoascus aurantiacus and its expression in yeast. Appl Microbiol Biotechnol, 2003, 63142-50

[41] BulakhovAG, VolkovPV, RozhkovaAM, GusakovAV, NemashkalovVA, SatrutdinovAD, SinitsynAP. Using an inducible promoter of a gene encoding Penicillium verruculosum glucoamylase for production of enzyme preparations with enhanced cellulase performance. PLoS ONE, 2017, 121e0170404

[42] YaoG, LiZ, GaoL, WuR, KanQ, LiuG, QuY. Redesigning the regulatory pathway to enhance cellulase production in Penicillium oxalicum. Biotechnol Biofuels, 2015, 811-7

[43] XueD, LinD, GongC, PengC, YaoS. Expression of a bifunctional cellulase with exoglucanase and endoglucanase activities to enhance the hydrolysis ability of cellulase from a marine Aspergillus niger. Process Biochem, 2017, 52: 115-122

[44] QuaxTE, ClaassensNJ, SöllD, van der OostJ. Codon bias as a means to fine-tune gene expression. Mol Cell, 2015, 592149-161

[45] AkcapinarGB, GulO, SezermanU. Effect of codon optimization on the expression of Trichoderma reesei endoglucanase I in Pichia pastoris. Biotechnol Prog, 2011, 2751257-1263

[46] FangH, XiaL. Heterologous expression and production of Trichoderma reesei cellobiohydrolase II in Pichia pastoris and the application in the enzymatic hydrolysis of corn stover and rice straw. Biomass Bioenergy, 2015, 78: 99-109

[47] PhadtareP, JoshiS, SatyanarayanaT. Recombinant thermo-alkali-stable endoglucanase of Myceliopthora thermophila BJA (rMt-egl): biochemical characteristics and applicability in enzymatic saccharification of agro-residues. Int J Biol Macromol, 2017, 104: 107-116

[48] PeiJ, PangQ, ZhaoL, FanS, ShiH. Thermoanaerobacterium thermosaccharolyticum β-glucosidase: a glucose-tolerant enzyme with high specific activity for cellobiose. Biotechnol Biofuels, 2012, 511

[49] CaoL, LiS, HuangX, QinZ, KongW, XieW, LiuY. Enhancing the thermostability of highly active and glucose-tolerant β-glucosidase Ks5A7 by directed evolution for good performance of three properties. J Agric Food Chem, 2018, 665013228-13235

[50] LiuM, XieW, XuH, GuJ, LvX, YuH, YeL. Directed evolution of an exoglucanase facilitated by a co-expressed β-glucosidase and construction of a whole engineered cellulase system in Escherichia coli. Biotechnol Lett, 2014, 3691801-1807

[51] GoedegebuurF, DankmeyerL, GualfettiP, KarkehabadiS, HanssonH, JanaS, HuynhV, KelemenBR, KruithofP, LarenasEA, TeunissenPJ. Improving the thermal stability of cellobiohydrolase Cel7A from Hypocrea jecorina by directed evolution. J Biol Chem, 2017, 2924217418-17430

[52] LarueK, MelgarM, MartinVJ. Directed evolution of a fungal β-glucosidase in Saccharomyces cerevisiae. Biotechnol Biofuels, 2016, 911-5

[53] WakaiS, NakashimaN, OginoC, TsutsumiH, HataY, KondoA. Modified expression of multi-cellulases in a filamentous fungus Aspergillus oryzae. Bioresour Technol, 2019, 276: 146-153

[54] LiL, HuangC, ZhaoF, DengT, LinY, ZhengS, LiangS, HanS. Improved production and characterization of Volvariella volvacea Endoglucanase 1 expressed in Pichia pastoris. Protein Expr Purif, 2018, 152: 107-113

[55] WangQ, ZhongC, XiaoH. Genetic engineering of filamentous fungi for efficient protein expression and secretion. Front Bioeng Biotechnol, 2020, 8: 293

[56] ZhuH, YaoS, WangS. MFα signal peptide enhances the expression of cellulase eg1 gene in yeast. Appl Biochem Biotechnol, 2010, 1623617-624

[57] InokumaK, BambaT, IshiiJ, ItoY, HasunumaT, KondoA. Enhanced cell-surface display and secretory production of cellulolytic enzymes with Saccharomyces cerevisiae Sed1 signal peptide. Biotechnol Bioeng, 2016, 113112358-2366

[58] BaeJH, SungBH, KimHJ, ParkSH, LimKM, KimMJ, LeeCR, SohnJH. An efficient genome-wide fusion partner screening system for secretion of recombinant proteins in yeast. Sci Rep, 2015, 511-5

[59] DadwalA, SharmaS, SatyanarayanaT. Progress in ameliorating beneficial characteristics of microbial cellulases by genetic engineering approaches for cellulose saccharification. Front Microbiol, 2020, 2020: 11

[60] XiaoS, ShiloachJ, BetenbaughMJ. Engineering cells to improve protein expression. Curr Opin Struct Biol, 2014, 26: 32-38

[61] TangH, BaoX, ShenY, SongM, WangS, WangC, HouJ. Engineering protein folding and translocation improves heterologous protein secretion in Saccharomyces cerevisiae. Biotechnol Bioeng, 2015, 11291872-1882

[62] Yang F, Yang X, Li Z, Du C, Wang J, Li S. Overexpression and characterization of a glucose-tolerant β-glucosidase from T. aotearoense with high specific activity for cellobiose. Appl Microbiol Biotechnol. 2015; 99(21):8903–15.

[63] Van ZylJH, Den HaanR, Van ZylWH. Over-expression of native Saccharomyces cerevisiae exocytic SNARE genes increased heterologous cellulase secretion. Appl Microbiol Biotechnol, 2014, 98125567-5578

[64] KuhadRC, DeswalD, SharmaS, BhattacharyaA, JainKK, KaurA, PletschkeBI, SinghA, KarpM. Revisiting cellulase production and redefining current strategies based on major challenges. Renew Sustain Energ Rev, 2016, 55: 249-272

[65] GreeneER, HimmelME, BeckhamGT, TanZ. Glycosylation of cellulases: engineering better enzymes for biofuels. Adv Carbohydr Chem Biochem, 2015, 72: 63-112

[66] ChungD, SaraiNS, KnottBC, HenggeN, RussellJF, YarbroughJM, BruneckyR, YoungJ, SupekarN, Vander WallT, SammondDW. Glycosylation is vital for industrial performance of hyperactive cellulases. ACS Sustain Chem Eng, 2019, 754792-4800

[67] AdneyWS, JeohT, BeckhamGT, ChouYC, BakerJO, MichenerW, HimmelME. Probing the role of N-linked glycans in the stability and activity of fungal cellobiohydrolases by mutational analysis. Cellulose, 2009, 164699-709

[68] GuptaR, BaldockSJ, FieldenPR, GrieveBD. Capillary zone electrophoresis for the analysis of glycoforms of cellobiohydrolase. J Chromatogr A, 2011, 1218315362-5368

[69] GuanX, ChaffeyPK, ZengC, GreeneER, ChenL, DrakeMR, ChenC, GroobmanA, ReschMG, HimmelME, BeckhamGT. Molecular-scale features that govern the effects of O-glycosylation on a carbohydrate-binding module. Chem Sci, 2015, 6127185-7189

[70] UllahM, XiaL, XieS, SunS. CRISPR/Cas9-based genome engineering: a new breakthrough in the genetic manipulation of filamentous fungi. Biotechnol Appl Biochem, 2020, 676835-851

[71] BaiSK, HongY, WuYR. Emerging technologies for genetic modification of solventogenic clostridia: from tool to strategy development. Bioresour Technol, 2021, 334125222

[72] IshinoY, KrupovicM, ForterreP. History of CRISPR-Cas from encounter with a mysterious repeated sequence to genome editing technology. J Bacteriol, 2018, 2007e00580-e617

[73] SongR, ZhaiQ, SunL, HuangE, ZhangY, ZhuY, GuoQ, TianY, ZhaoB, LuH. CRISPR/Cas9 genome editing technology in filamentous fungi: progress and perspective. Appl Microbiol Biotechnol, 2019, 103176919-6932

[74] SternbergSH, ReddingS, JinekM, GreeneEC, DoudnaJA. DNA interrogation by the CRISPR RNA-guided endonuclease Cas9. Nature, 2014, 507749062-67

[75] YaoR, LiuD, JiaX, ZhengY, LiuW, XiaoY. CRISPR-Cas9/Cas12a biotechnology and application in bacteria. Synth Syst Biotechnol, 2018, 33135-149

[76] Matsu-UraT, BaekM, KwonJ, HongC. Efficient gene editing in Neurospora crassa with CRISPR technology. Fungal Biol Biotechnol, 2015, 211-7

[77] ZhangC, MengX, WeiX, LuL. Highly efficient CRISPR mutagenesis by microhomology-mediated end joining in Aspergillus fumigatus. Fungal Genet Biol, 2016, 86: 47-57

[78] DengH, GaoR, LiaoX, CaiY. CRISPR system in filamentous fungi: current achievements and future directions. Gene, 2017, 627: 212-221

[79] WangQ, ColemanJJ. Progress and challenges: development and implementation of CRISPR/CAS9 technology in filamentous fungi. Comput Struct Biotechnol J, 2019, 17: 761-769

[80] KatayamaT, TanakaY, OkabeT, NakamuraH, FujiiW, KitamotoK, MaruyamaJI. Development of a genome editing technique using the CRISPR/Cas9 system in the industrial filamentous fungus Aspergillus oryzae. Biotechnol Lett, 2016, 384637-642

[81] ShiTQ, LiuGN, JiRY, ShiK, SongP, RenLJ, HuangH, JiXJ. CRISPR/Cas9-based genome editing of the filamentous fungi: the state of the art. Appl Microbiol Biotechnol, 2017, 101207435-7443

[82] GaoY, ZhaoY. Self-processing of ribozyme-flanked RNAs into guide RNAs in vitro and in vivo for CRISPR-mediated genome editing. J Integr Plant Biol, 2014, 564343-349

[83] NissimL, PerliSD, FridkinA, Perez-PineraP, LuTK. Multiplexed and programmable regulation of gene networks with an integrated RNA and CRISPR/Cas toolkit in human cells. Mol Cell, 2014, 544698-710

[84] ZhengX, ZhengP, ZhangK, CairnsTC, MeyerV, SunJ, MaY. 5S rRNA promoter for guide RNA expression enabled highly efficient CRISPR/Cas9 genome editing in Aspergillus niger. ACS Synth Biol, 2018, 871568-1574

[85] MaX, ZhuQ, ChenY, LiuYG. CRISPR/Cas9 platforms for genome editing in plants: developments and applications. Mol Plant, 2016, 97961-974

[86] ShalemO, SanjanaNE, ZhangF. High-throughput functional genomics using CRISPR–Cas9. Nat Rev Genet, 2015, 165299-311

[87] BranzeiD, FoianiM. Regulation of DNA repair throughout the cell cycle. Nat Rev Mol Cell Biol, 2008, 94297-308

[88] FengZ, MaoY, XuN, ZhangB, WeiP, YangDL, WangZ, ZhangZ, ZhengR, YangL, ZengL. Multigeneration analysis reveals the inheritance, specificity, and patterns of CRISPR/Cas-induced gene modifications in Arabidopsis. Proc Natl Acad Sci USA, 2014, 111124632-4637

[89] LiuR, ChenL, JiangY, ZhouZ, ZouG. Efficient genome editing in filamentous fungus Trichoderma reesei using the CRISPR/Cas9 system. Cell Discov, 2015, 111-1

[90] LiuQ, GaoR, LiJ, LinL, ZhaoJ, SunW, TianC. Development of a genome-editing CRISPR/Cas9 system in thermophilic fungal Myceliophthora species and its application to hyper-cellulase production strain engineering. Biotechnol Biofuels, 2017, 1011-4

[91] YangP, WuY, ZhengZ, CaoL, ZhuX, MuD, JiangS. CRISPR-Cas9 approach constructing cellulase sestc-engineered Saccharomyces cerevisiae for the production of orange peel ethanol. Front Microbiol, 2018, 9: 2436

[92] AbdulrachmanD, EurwilaichitrL, ChampredaV, ChantasinghD, PootanakitK. Development of a CRISPR/Cpf1 system for targeted gene disruption in Aspergillus aculeatus TBRC 277. BMC Biotechnol, 2021, 2111-13

[93] AlokA, SandhyaD, JogamP, RodriguesV, BhatiKK, SharmaH, KumarJ. The rise of the CRISPR/Cpf1 system for efficient genome editing in plants. Front Plant Sci, 2020, 11: 264

[94] OuedraogoJP, TsangA. CRISPR-Cas systems for fungal research. Fungal Biol Rev, 2020, 344189-201

[95] Adiego-PérezB, RandazzoP, DaranJM, VerwaalR, RoubosJA, Daran-LapujadeP, Van Der OostJ. Multiplex genome editing of microorganisms using CRISPR-Cas. FEMS Microbiol Lett, 2019, 3668fnz086

[96] SinghA, PatelAK, AdsulM, MathurA, SinghaniaRR. Genetic modification: a tool for enhancing cellulase secretion. Biofuel Res J, 2017, 42600-610

[97] GuazzaroniME, PlateroRA, Silva-RochaR. Genomic and postgenomic approaches to understand environmental microorganisms. Int J Genomics, 2018.

[98] XueY, HanJ, LiY, LiuJ, GanL, LongM. Promoting cellulase and hemicellulase production from Trichoderma orientalis EU7–22 by overexpression of transcription factors Xyr1 and Ace3. Bioresour Technol, 2020, 296122355

[99] WangL, LvX, CaoY, ZhengF, MengX, ShenY, ChenG, LiuW, ZhangW. A novel transcriptional regulator RXE1 modulates the essential transactivator XYR1 and cellulase gene expression in Trichoderma reesei. Appl Microbiol Biotechnol, 2019, 103114511-4523

[100] CaoY, ZhengF, WangL, ZhaoG, ChenG, ZhangW, LiuW. Rce1, a novel transcriptional repressor, regulates cellulase gene expression by antagonizing the transactivator Xyr1 in Trichoderma reesei. Mol Microbiol, 2017, 105165-83

[101] LiuP, LinA, ZhangG, ZhangJ, ChenY, ShenT, ZhaoJ, WeiD, WangW. Enhancement of cellulase production in Trichoderma reesei RUT-C30 by comparative genomic screening. Microb Cell Fact, 2019, 18181

[102] MhuantongW, CharoensriS, PoonsrisawatA, PootakhamW, TangphatsornruangS, SiamphanC, SuwannarangseeS, EurwilaichitrL, ChampredaV, CharoensawanV, ChantasinghD. High quality Aspergillus aculeatus genomes and transcriptomes: a platform for cellulase activity optimization toward industrial applications. Front Bioeng Biotechnol, 2021, 8607176

[103] LuoY, ValkonenM, JacksonRE, PalmerJM, BhallaA, NikolaevI, SaloheimoM, WardM. Modification of transcriptional factor ACE3 enhances protein production in Trichoderma reesei in the absence of cellulase gene inducer. Biotechnol Biofuels, 2020, 1311-16

[104] HanL, LiuK, MaW, JiangY, HouS, TanY, YuanQ, NiuK, FangX. Redesigning transcription factor Cre1 for alleviating carbon catabolite repression in Trichoderma reesei. Synth Syst Biotechnol, 2020, 53230-235

[105] Martins-SantanaL, PaulaRGD, SilvaAG, LopesDCB, SilvaRDN, Silva-RochaR. CRZ1 regulator and calcium cooperatively modulate holocellulases gene expression in Trichoderma reesei QM6a. Genet Mol Biol, 2020, 432e20190244

[106] MengQS, ZhangF, LiuCG, ZhaoXQ, BaiFW. Identification of a novel repressor encoded by the putative gene ctf1 for cellulase biosynthesis in Trihoderma reesei through artificial zinc finger engineering. Biotechnol Bioeng, 2020, 11761747-1760

[107] SamalA, CraigJP, CoradettiST, BenzJP, EddyJA, PriceND, GlassNL. Network reconstruction and systems analysis of plant cell wall deconstruction by Neurospora crassa. Biotechnol Biofuels, 2017, 1011-21

[108] HubermanLB, CoradettiST, GlassNL. Network of nutrient-sensing pathways and a conserved kinase cascade integrate osmolarity and carbon sensing in Neurospora crassa. Proc Natl Acad Sci USA, 2017, 11441E8665-E8674

[109] KimJE, NamH, ParkJ, ChoiGJ, LeeYW, SonH. Characterization of the CCAAT-binding transcription factor complex in the plant pathogenic fungus Fusarium graminearum. Sci Rep, 2020, 1011-11

[110] BayramÖS, DettmannA, KarahodaB, MoloneyNM, OrmsbyT, McGowanJ, Cea-SánchezS, Miralles-DuránA, BranciniGT, LuqueEM, FitzpatrickDA. Control of development, secondary metabolism and light-dependent carotenoid biosynthesis by the velvet complex of Neurospora crassa. Genetics, 2019, 2123691-710

[111] ZhaoS, LiaoXZ, WangJX, NingYN, LiCX, LiaoLS, LiuQ, JiangQ, GuLS, FuLH, YanYS. Transcription factor Atf1 regulates expression of cellulase and xylanase genes during solid-state fermentation of ascomycetes. Appl Env Microbiol, 2019, 8524e01226-19

[112] YaoG, LiZ, WuR, QinY, LiuG, QuY. Penicillium oxalicum PoFlbC regulates fungal asexual development and is important for cellulase gene expression. Fungal Genet Biol, 2016, 86: 91-102

[113] ZhaoS, LiuQ, WangJX, LiaoXZ, GuoH, LiCX, ZhangFF, LiaoLS, LuoXM, FengJX. Differential transcriptomic profiling of filamentous fungus during solid-state and submerged fermentation and identification of an essential regulatory gene PoxMBF1 that directly regulated cellulase and xylanase gene expression. Biotechnol Biofuels, 2019, 1211-4

[114] SchmollM. Regulation of plant cell wall degradation by light in Trichoderma. Fungal Biol Biotechnol, 2018, 511-20

[115] AntonietoAC, NogueiraKM, de PaulaRG, NoraLC, CassianoMH, GuazzaroniME, AlmeidaF, da SilvaTA, RiesLN, de AssisLJ, GoldmanGH. A novel Cys2His2 zinc finger homolog of AZF1 modulates holocellulase expression in Trichoderma reesei. mSystems, 2019, 44e00161-19

[116] LiY, HuY, ZhuZ, ZhaoK, LiuG, WangL, QuY, ZhaoJ, QinY. Normal transcription of cellulolytic enzyme genes relies on the balance between the methylation of H3K36 and H3K4 in Penicillium oxalicum. Biotechnol Biofuels, 2019, 1211-19

[117] ZhengF, CaoY, WangL, LvX, MengX, ZhangW, ChenG, LiuW. The mating type locus protein MAT1-2-1 of Trichoderma reesei interacts with Xyr1 and regulates cellulase gene expression in response to light. Sci Rep, 2017, 711-3

[118] Wang Y, Liu R, Liu H, Li X, Shen L, Zhang W, Song X, Liu W, Liu X, Zhong Y (2021) Development of a powerful synthetic hybrid promoter to improve the cellulase system of Trichoderma Reesei for efficient saccharification of corncob residues. 09 June 2021, PREPRINT (Version 1) available at Research Square https://doi.org/10.21203/rs.3.rs-584234/v1

[119] SunX, XueX, LiM, GaoF, HaoZ, HuangH, LuoH, QinL, YaoB, SuX. Efficient coproduction of mannanase and cellulase by the transformation of a codon-optimized endomannanase gene from Aspergillus niger into Trichoderma reesei. J Agric Food Chem, 2017, 655011046-11053

[120] MiaoT, BasitA, WenJ, LiuJ, ZhengF, CaoY, JiangW. High efficient degradation of glucan/glucomannan to cello-/mannan-oligosaccharide by endoglucanase via tetrasaccharide as intermediate. Food Chem, 2021, 350129175

[121] AkbarzadehA, PourzardoshtN, DehnaviE, SiadatSOR, ZamaniMR, MotallebiM, JamnaniFN, AghaeepoorM, TashniziMB. Disulfide bonds elimination of endoglucanase II from Trichoderma reesei by site-directed mutagenesis to improve enzyme activity and thermal stability: an experimental and theoretical approach. Int J Biol Macromol, 2018, 120: 1572-1580

[122] TangH, SongM, HeY, WangJ, WangS, ShenY, HouJ, BaoX. Engineering vesicle trafficking improves the extracellular activity and surface display efficiency of cellulases in Saccharomyces cerevisiae. Biotechnol Biofuels, 2017, 1011-13

[123] ManglekarRR, GengA. CRISPR-Cas9-mediated seb1 disruption in Talaromyces pinophilus EMU for its enhanced cellulase production. Enzyme Microb Technol, 2020, 140109646

[124] AdewumiIK, OgedengbeMO, AdepetuJA, AinaPO. Aerobic composting of municipal solid wastes and poultry manure. J Appl Sci Res, 2005, 1: 292-297

[125] BoaseNA, KellyJM. A role for creD, a carbon catabolite repression gene from Aspergillus nidulans, in ubiquitination. Mol Microbiol, 2004, 533929-940

[126] BrownB, AaronMSmithJ. The politics of nature. The rise of modern genomics, 20013New YorkWiley230-257

[127] CarrollA, SomervilleC. Cellulosic biofuels. Annu Rev Plant Biol, 2009, 60: 165-182

[128] DasA, PaulT, JanaA, HalderSK, GhoshK, MaityC, Das MohapatraPK, PatiBR, MondalKC. Bioconversion of rice straw to sugar using multizyme complex of fungal origin and subsequent production of bioethanol by mixed fermentation of Saccharomyces cerevisiae MTCC 173 and Zymomonas mobilis MTCC 2428. Ind Crops Prod, 2013, 46: 217-225

[129] de VriesRP, VisserJA. Aspergillus enzymes involved in degradation of plant cell wall polysaccharides. Microbiol Mol Biol Rev, 2001, 654497-522

[130] HäkkinenM, ValkonenMJ, Westerholm-ParvinenA, AroN, ArvasM, VitikainenM, PenttiläM, SaloheimoM, PakulaTM. Screening of candidate regulators for cellulase and hemicellulase production in Trichoderma reesei and identification of a factor essential for cellulase production. Biotechnol Biofuels, 2014, 711-21

[131] JägerG, GirfoglioM, DolloF, RinaldiR, BongardH, CommandeurU, FischerR, SpiessAC, BüchsJ. How recombinant swollenin from Kluyveromyces lactis affects cellulosic substrates and accelerates their hydrolysis. Biotechnol Biofuels, 2011, 411-6

[132] Le RhunA, Escalera-MaurerA, BratovičM, CharpentierE. CRISPR-Cas in Streptococcus pyogenes. RNA Biol, 2019, 164380-389

[133] LiJ, ZhangY, LiJ, SunT, TianC. Metabolic engineering of the cellulolytic thermophilic fungus Myceliophthora thermophila to produce ethanol from cellobiose. Biotechnol Biofuels, 2020, 13123

[134] LiYL, LiH, LiAN, LiDC. Cloning of a gene encoding thermostable cellobiohydrolase from the thermophilic fungus Chaetomium thermophilum and its expression in Pichia pastoris. J Appl Microbiol, 2009, 10661867-1875

[135] ManoliMT, EspesoEA. Modulation of calcineurin activity in Aspergillus nidulans: the roles of high magnesium concentrations and of transcriptional factor CrzA. Mol Microbiol, 2019, 11151283-1301

[136] MoonSB, LeeJM, KangJG, LeeNE, HaDI, KimSH, YooK, KimD, KoJH, KimYS. Highly efficient genome editing by CRISPR-Cpf1 using CRISPR RNA with a uridinylate-rich 3′-overhang. Nat Commun, 2018, 911-11

[137] NittaM, FurukawaT, ShidaY, MoriK, KuharaS, MorikawaY, OgasawaraW. A new Zn (II) 2Cys6-type transcription factor BglR regulates β-glucosidase expression in Trichoderma reesei. Fungal Genet Biol, 2012, 495388-397

[138] PanchapakesanA, ShankarNGuptaV. Fungal cellulases: an overview. New and future developments in microbial biotechnology and bioengineering, 2016Elsevier9-18

[139] PrabhuRR, ParasharD, SatyanarayanaT. Production and characteristics of the recombinant extracellular bifunctional endoglucanase of the polyextremophilic bacterium Bacillus halodurans and its applicability in saccharifying agro-residues. Bioprocess Biosyst Eng, 2017, 405651-662

[140] RahmanZ, ShidaY, FurukawaT, SuzukiY, OkadaH, OgasawaraW, MorikawaY. Application of Trichoderma reesei cellulase and xylanase promoters through homologous recombination for enhanced production of extracellular β-glucosidase I. Biosci Biotechnol Biochem, 2009, 7351083-1089

[141] SunFF, BaiR, YangH, WangF, HeJ, WangC, TuM. Heterologous expression of codon optimized Trichoderma reesei Cel6A in Pichia pastoris. Enzyme Microb Technol, 2016, 92: 107-116

[142] ThakurMK, ThakurVK, GuptaRK, PappuA. Synthesis and applications of biodegradable soy based graft copolymers: a review. ACS Sustain Chem Eng, 2016, 411-7

[143] ToddRB, ZhouM, OhmRA, LeeggangersHA, VisserL, De VriesRP. Prevalence of transcription factors in ascomycete and basidiomycete fungi. BMC Genomics, 2014, 1511-2

[144] Vázquez-MontoyaEL, Castro-OchoaLD, Maldonado-MendozaIE, Luna-SuárezS, Castro-MartínezC. Moringa straw as cellulase production inducer and cellulolytic fungi source. Rev Argent Microbiol, 2020, 5214-12

[145] WeiY, ZhouH, ZhangJ, ZhangL, GengA, LiuF, ZhaoG, WangS, ZhouZ, YanX. Insight into dominant cellulolytic bacteria from two biogas digesters and their glycoside hydrolase genes. PLoS ONE, 2015, 106e0129921

[146] XiaoH, BaoZ, ZhaoH. High throughput screening and selection methods for directed enzyme evolution. Ind Eng Chem Res, 2015, 54164011-4020

[147] Srivastava N, Elgorban AM, Mishra PK, Marraiki N, Alharbi AM,Ahmad I, Gupta VK. Enhance production of fungal cellulase cocktail using cellulosic waste. Environ Technol Inno.2020; 19:100949.

[148] Singhania RR, Sukumaran RK, Patel AK, Larroche C, Pandey A. Advancement and comparative profiles in the production technologies using solid-state and submerged fermentation for microbialcellulases. Enzyme Microb Technol. 2010;46(7):541-9.

[149] Zou G, Shi S, Jiang Y, van den BrinkJ, de Vries RP, Chen L, Zhang J, Ma L, Wang C, Zhou Z. Construction of a cellulase hyper-expression system inTrichoderma reesei by promoter and enzyme engineering. Microb Cell Fact. 2012;11(1):1-2.

[150] Bower BS, Larenas EA, Mitchinson C.Exo-endo cellulase fusion protein. WO Patent WO2005093073. 2005.

[151] Liu D, Zhang R, Yang X, Zhang Z,Song S, Miao Y, Shen Q. Characterization of a thermostable β-glucosidase from Aspergillus fumigatus Z5, and itsfunctional expression in Pichia pastoris X33. Microb Cell Fact. 2012;11(1):1-5.

[152] Packer MS, Liu DR. Methods for the directed evolution ofproteins. Nat Rev Gen. 2015;16(7):379-94

[153] Payne CM, Resch MG, Chen L, Crowley MF, Himmel ME, Taylor LE,Sandgren M, Ståhlberg J, Stals I, Tan Z, Beckham GT. Glycosylated linkers in multimodular lignocellulosedegradingenzymes dynamically bind to cellulose. PNAS. 2013;110(36):14646-51.

[154] Wei W, Chen L, Zou G,Wang Q, Yan X, Zhang J, Wang C, Zhou Z. N-glycosylation affects the proper folding, enzymatic characteristicsand production of a fungal β-glucosidase. Biotechnol Bioeng. 2013;110(12):3075-84.

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