Abstract
Trichoderma atroviride and Trichoderma harzianum are widely used as commercial biocontrol agents against plant diseases. Recently, T. harzianum IOC-3844 (Th3844) and T. harzianum CBMAI-0179 (Th0179) demonstrated great potential in the enzymatic conversion of lignocellulose into fermentable sugars. Herein, we performed whole-genome sequencing and assembly of the Th3844 and Th0179 strains. To assess the genetic diversity within the genus Trichoderma, the results of both strains were compared with strains of T. atroviride CBMAI-00020 (Ta0020) and T. reesei CBMAI-0711 (Tr0711). The sequencing coverage value of all genomes evaluated in this study was higher than that of previously reported genomes for the same species of Trichoderma. The resulting assembly revealed total lengths of 40 Mb (Th3844), 39 Mb (Th0179), 36 Mb (Ta0020), and 32 Mb (Tr0711). A genome-wide phylogenetic analysis provided details on the relationships of the newly sequenced species with other Trichoderma species. Structural variants revealed genomic rearrangements among Th3844, Th0179, Ta0020, and Tr0711 relative to the T. reesei QM6a reference genome and showed the functional effects of such variants. In conclusion, the findings presented herein allow the visualization of genetic diversity in the evaluated strains and offer opportunities to explore such fungal genomes in future biotechnological and industrial applications.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
All data generated or analyzed in this study are included in this published article (and its supplementary information files). The raw datasets and the assembled genomes were deposited in the NCBI Sequence Read Archive and can be accessed under BioProject number PRJNA781962 and BioSample number as follows: SAMN23309297 (Th3844), SAMN23309298 (Th0179), SAMN23309299 (Ta0020), and SAMN23309300 (Tr0711).
References
Afgan E, Baker D, Batut B, van den Beek M, Bouvier D, Cech M, Chilton J, Clements D, Coraor N, Gruning BA, Guerler A, Hillman-Jackson J, Hiltemann S, Jalili V, Rasche H, Soranzo N, Goecks J, Taylor J, Nekrutenko A, Blankenberg D (2018) The galaxy platform for accessible, reproducible and collaborative biomedical analyses: 2018 update. Nucleic Acids Res 46:W537–W544. https://doi.org/10.1093/nar/gky379
Almeida DA, Horta MAC, Ferreira Filho JA, Murad NF, de Souza AP (2021) The synergistic actions of hydrolytic genes reveal the mechanism of Trichoderma harzianum for cellulose degradation. J Biotechnol 334:1–10. https://doi.org/10.1016/j.jbiotec.2021.05.001
Amore A, Knott BC, Supekar NT, Shajahan A, Azadi P, Zhao P, Wells L, Linger JG, Hobdey SE, Vander Wall TA, Shollenberger T, Yarbrough JM, Tan Z, Crowley MF, Himmel ME, Decker SR, Beckham GT, Taylor LE (2017) Distinct roles of N- and O-glycans in cellulase activity and stability. Proc Natl Acad Sci U S A 114:13667–13672. https://doi.org/10.1073/pnas.1714249114
Andersen MR, Salazar MP, Schaap PJ, van de Vondervoort PJ, Culley D, Thykaer J, Frisvad JC, Nielsen KF, Albang R, Albermann K, Berka RM, Braus GH, Braus-Stromeyer SA, Corrochano LM, Dai Z, van Dijck PW, Hofmann G, Lasure LL, Magnuson JK, Menke H, Meijer M, Meijer SL, Nielsen JB, Nielsen ML, van Ooyen AJ, Pel HJ, Poulsen L, Samson RA, Stam H, Tsang A, van den Brink JM, Atkins A, Aerts A, Shapiro H, Pangilinan J, Salamov A, Lou Y, Lindquist E, Lucas S, Grimwood J, Grigoriev IV, Kubicek CP, Martinez D, van Peij NN, Roubos JA, Nielsen J, Baker SE (2011) Comparative genomics of citric-acid-producing Aspergillus niger ATCC 1015 versus enzyme-producing CBS 513.88. Genome Res 21:885–897. https://doi.org/10.1101/gr.112169.110
Ardui S, Ameur A, Vermeesch JR, Hestand MS (2018) Single molecule real-time (SMRT) sequencing comes of age: applications and utilities for medical diagnostics. Nucleic Acids Res 46:2159–2168. https://doi.org/10.1093/nar/gky066
Arntzen MO, Bengtsson O, Varnai A, Delogu F, Mathiesen G, Eijsink VGH (2020) Quantitative comparison of the biomass-degrading enzyme repertoires of five filamentous fungi. Sci Rep 10:20267. https://doi.org/10.1038/s41598-020-75217-z
Baroncelli R, Piaggeschi G, Fiorini L, Bertolini E, Zapparata A, Pe ME, Sarrocco S, Vannacci G (2015) Draft whole-genome sequence of the biocontrol agent Trichoderma harzianum T6776. Genome Announc. https://doi.org/10.1128/genomeA.00647-15
Beckham GT, Dai Z, Matthews JF, Momany M, Payne CM, Adney WS, Baker SE, Himmel ME (2012) Harnessing glycosylation to improve cellulase activity. Curr Opin Biotechnol 23:338–345. https://doi.org/10.1016/j.copbio.2011.11.030
Bischof RH, Ramoni J, Seiboth B (2016) Cellulases and beyond: the first 70 years of the enzyme producer Trichoderma reesei. Microb Cell Fact 15:106. https://doi.org/10.1186/s12934-016-0507-6
Blin K, Shaw S, Kloosterman AM, Charlop-Powers Z, van Wezel GP, Medema MH, Weber T (2021) antiSMASH 6.0: improving cluster detection and comparison capabilities. Nucleic Acids Res 49:W29–W35. https://doi.org/10.1093/nar/gkab335
Brakhage AA (2013) Regulation of fungal secondary metabolism. Nat Rev Microbiol 11:21–32. https://doi.org/10.1038/nrmicro2916
Buchfink B, Xie C, Huson DH (2015) Fast and sensitive protein alignment using DIAMOND. Nat Methods 12:59–60. https://doi.org/10.1038/nmeth.3176
Busk PK, Pilgaard B, Lezyk MJ, Meyer AS, Lange L (2017) Homology to peptide pattern for annotation of carbohydrate-active enzymes and prediction of function. BMC Bioinformatics 18:214. https://doi.org/10.1186/s12859-017-1625-9
Cantalapiedra CP, Hernández-Plaza A, Letunic I, Bork P, Huerta-Cepas J (2021) eggNOG-mapper v2: functional annotation, orthology assignments, and domain prediction at the metagenomic scale. bioRxiv. https://doi.org/10.1101/2021.06.03.446934
Cantarel BL, Korf I, Robb SM, Parra G, Ross E, Moore B, Holt C, Alvarado AS, Yandell M (2008) MAKER: an easy-to-use annotation pipeline designed for emerging model organism genomes. Genome Res 18:188–196. https://doi.org/10.1101/gr.6743907
Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B (2009) The carbohydrate-active enzymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res 37:D233–D238. https://doi.org/10.1093/nar/gkn663
Chaverri P, Branco-Rocha F, Jaklitsch W, Gazis R, Degenkolb T, Samuels GJ (2015) Systematics of the Trichoderma harzianum species complex and the re-identification of commercial biocontrol strains. Mycologia 107:558–590. https://doi.org/10.3852/14-147
Chen M, Liu Q, Gao SS, Young AE, Jacobsen SE, Tang Y (2019) Genome mining and biosynthesis of a polyketide from a biofertilizer fungus that can facilitate reductive iron assimilation in plant. Proc Natl Acad Sci U S A 116:5499–5504. https://doi.org/10.1073/pnas.1819998116
Chung D, Kwon YM, Yang Y (2021) Telomere-to-telomere genome assembly of asparaginase-producing Trichoderma simmonsii. BMC Genom 22:830. https://doi.org/10.1186/s12864-021-08162-4
Cingolani P, Platts A, le Wang L, Coon M, Nguyen T, Wang L, Land SJ, Lu X, Ruden DM (2012) A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly (austin) 6:80–92. https://doi.org/10.4161/fly.19695
Correa CL, Midorikawa GEO, Filho EXF, Noronha EF, Alves GSC, Togawa RC, Silva-Junior OB, Costa M, Grynberg P, Miller RNG (2020) Transcriptome profiling-based analysis of carbohydrate-active enzymes in aspergillus terreus involved in plant biomass degradation. Front Bioeng Biotechnol. https://doi.org/10.3389/fbioe.2020.564527
Couturier M, Ladeveze S, Sulzenbacher G, Ciano L, Fanuel M, Moreau C, Villares A, Cathala B, Chaspoul F, Frandsen KE, Labourel A, Herpoel-Gimbert I, Grisel S, Haon M, Lenfant N, Rogniaux H, Ropartz D, Davies GJ, Rosso MN, Walton PH, Henrissat B, Berrin JG (2018) Lytic xylan oxidases from wood-decay fungi unlock biomass degradation. Nat Chem Biol 14:306–310. https://doi.org/10.1038/nchembio.2558
Crucello A, Sforca DA, Horta MA, dos Santos CA, Viana AJ, Beloti LL, de Toledo MA, Vincentz M, Kuroshu RM, de Souza AP (2015) Analysis of genomic regions of Trichoderma harzianum IOC-3844 related to biomass degradation. PLoS ONE. https://doi.org/10.1371/journal.pone.0122122
Dana CM, Dotson-Fagerstrom A, Roche CM, Kal SM, Chokhawala HA, Blanch HW, Clark DS (2014) The importance of pyroglutamate in cellulase cel7a. Biotechnol Bioeng 111:842–847. https://doi.org/10.1002/bit.25178
de Vries RP, Riley R, Wiebenga A, Aguilar-Osorio G, Amillis S, Uchima CA, Anderluh G, Asadollahi M, Askin M, Barry K, Battaglia E, Bayram O, Benocci T, Braus-Stromeyer SA, Caldana C, Canovas D, Cerqueira GC, Chen F, Chen W, Choi C, Clum A, Dos Santos RA, Damasio AR, Diallinas G, Emri T, Fekete E, Flipphi M, Freyberg S, Gallo A, Gournas C, Habgood R, Hainaut M, Harispe ML, Henrissat B, Hilden KS, Hope R, Hossain A, Karabika E, Karaffa L, Karanyi Z, Krasevec N, Kuo A, Kusch H, LaButti K, Lagendijk EL, Lapidus A, Levasseur A, Lindquist E, Lipzen A, Logrieco AF, MacCabe A, Makela MR, Malavazi I, Melin P, Meyer V, Mielnichuk N, Miskei M, Molnar AP, Mule G, Ngan CY, Orejas M, Orosz E, Ouedraogo JP, Overkamp KM, Park HS, Perrone G, Piumi F, Punt PJ, Ram AF, Ramon A, Rauscher S, Record E, Riano-Pachon DM, Robert V, Rohrig J, Ruller R, Salamov A, Salih NS, Samson RA, Sandor E, Sanguinetti M, Schutze T, Sepcic K, Shelest E, Sherlock G, Sophianopoulou V, Squina FM, Sun H, Susca A, Todd RB, Tsang A, Unkles SE, van de Wiele N, van Rossen-Uffink D, Oliveira JV, Vesth TC, Visser J, Yu JH, Zhou M, Andersen MR, Archer DB, Baker SE, Benoit I, Brakhage AA, Braus GH, Fischer R, Frisvad JC, Goldman GH, Houbraken J, Oakley B, Pocsi I, Scazzocchio C, Seiboth B, vanKuyk PA, Wortman J, Dyer PS, Grigoriev IV (2017) Comparative genomics reveals high biological diversity and specific adaptations in the industrially and medically important fungal genus Aspergillus. Genome Biol 18:28. https://doi.org/10.1186/s13059-017-1151-0
Delabona PDS, Codima CA, Ramoni J, Zubieta MP, de Araujo BM, Farinas CS, Pradella J, Seiboth B (2020) The impact of putative methyltransferase overexpression on the Trichoderma harzianum cellulolytic system for biomass conversion. Bioresour Technol. https://doi.org/10.1016/j.biortech.2020.123616
Dodd SL, Lieckfeldt E, Samuels GJ (2003) Hypocrea atroviridis sp. nov., the teleomorph of Trichoderma atroviride. Mycologia 95:27–40. https://doi.org/10.1080/15572536.2004.11833129
Druzhinina IS, Kopchinskiy AG, Kubicek CP (2006) The first 100 Trichoderma species characterized by molecular data. Mycoscience 47:55–64. https://doi.org/10.1007/s10267-006-0279-7
Druzhinina IS, Kubicek CP, Komon-Zelazowska M, Mulaw TB, Bissett J (2010) The Trichoderma harzianum demon: complex speciation history resulting in coexistence of hypothetical biological species, recent agamospecies and numerous relict lineages. BMC Evol Biol 10:94. https://doi.org/10.1186/1471-2148-10-94
Druzhinina IS, Chenthamara K, Zhang J, Atanasova L, Yang D, Miao Y, Rahimi MJ, Grujic M, Cai F, Pourmehdi S, Salim KA, Pretzer C, Kopchinskiy AG, Henrissat B, Kuo A, Hundley H, Wang M, Aerts A, Salamov A, Lipzen A, LaButti K, Barry K, Grigoriev IV, Shen Q, Kubicek CP (2018) Massive lateral transfer of genes encoding plant cell wall-degrading enzymes to the mycoparasitic fungus Trichoderma from its plant-associated hosts. PLoS Genet. https://doi.org/10.1371/journal.pgen.1007322
Emms DM, Kelly S (2015) OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biol 16:157. https://doi.org/10.1186/s13059-015-0721-2
Emms DM, Kelly S (2017) STRIDE: species tree root inference from gene duplication events. Mol Biol Evol 34:3267–3278. https://doi.org/10.1093/molbev/msx259
Emms DM, Kelly S (2018) STAG: species tree inference from all genes. bioRxiv. https://doi.org/10.1101/267914
Emms DM, Kelly S (2019) OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biol 20:238. https://doi.org/10.1186/s13059-019-1832-y
Fanelli F, Liuzzi VC, Logrieco AF, Altomare C (2018) Genomic characterization of Trichoderma atrobrunneum (T. harzianum species complex) ITEM 908: insight into the genetic endowment of a multi-target biocontrol strain. BMC Genom. https://doi.org/10.1186/s12864-018-5049-3
Fang H, Li C, Zhao J, Zhao C (2021) Biotechnological advances and trends in engineering Trichoderma reesei towards cellulase hyperproducer. Biotechnol Bioprocess Eng 26:517–528. https://doi.org/10.1007/s12257-020-0243-y
Filho JAF, Horta MAC, Beloti LL, Dos Santos CA, de Souza AP (2017) Carbohydrate-active enzymes in Trichoderma harzianum: a bioinformatic analysis bioprospecting for key enzymes for the biofuels industry. BMC Genom 18:779. https://doi.org/10.1186/s12864-017-4181-9
Finn RD, Clements J, Eddy SR (2011) HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 39:W29–W37. https://doi.org/10.1093/nar/gkr367
Fraceto LF, Maruyama CR, Guilger M, Mishra S, Keswani C, Singh HB, de Lima R (2018) Trichoderma harzianum-based novel formulations: potential applications for management of next-gen agricultural challenges. J Chem Technol Biotechnol 93:2056–2063. https://doi.org/10.1002/jctb.5613
Guo B, Sato N, Biely P, Amano Y, Nozaki K (2016) Comparison of catalytic properties of multiple beta-glucosidases of Trichoderma reesei. Appl Microbiol Biotechnol 100:4959–4968. https://doi.org/10.1007/s00253-016-7342-x
Gurevich A, Saveliev V, Vyahhi N, Tesler G (2013) QUAST: quality assessment tool for genome assemblies. Bioinformatics 29:1072–1075. https://doi.org/10.1093/bioinformatics/btt086
Hagestad OC, Hou L, Andersen JH, Hansen EH, Altermark B, Li C, Kuhnert E, Cox RJ, Crous PW, Spatafora JW, Lail K, Amirebrahimi M, Lipzen A, Pangilinan J, Andreopoulos W, Hayes RD, Ng V, Grigoriev IV, Jackson SA, Sutton TDS, Dobson ADW, Rama T (2021) Genomic characterization of three marine fungi, including Emericellopsis atlantica sp. nov. with signatures of a generalist lifestyle and marine biomass degradation. IMA Fungus. https://doi.org/10.1186/s43008-021-00072-0
Han L, Tan Y, Ma W, Niu K, Hou S, Guo W, Liu Y, Fang X (2020) Precision engineering of the transcription factor Cre1 in Hypocrea jecorina (Trichoderma reesei) for efficient cellulase production in the presence of glucose. Front Bioeng Biotechnol 8:852. https://doi.org/10.3389/fbioe.2020.00852
Horta MA, Vicentini R, Delabona Pda S, Laborda P, Crucello A, Freitas S, Kuroshu RM, Polikarpov I, Pradella JG, Souza AP (2014) Transcriptome profile of Trichoderma harzianum IOC-3844 induced by sugarcane bagasse. PLoS ONE. https://doi.org/10.1371/journal.pone.0088689
Horta MAC, Filho JAF, Murad NF, Santos EDO, Santos CAD, Mendes JS, Brandao MM, Azzoni SF, de Souza AP (2018) Network of proteins, enzymes and genes linked to biomass degradation shared by Trichoderma species. Sci Rep 8:1341. https://doi.org/10.1038/s41598-018-19671-w
Horta MAC, Thieme N, Gao Y, Burnum-Johnson KE, Nicora CD, Gritsenko MA, Lipton MS, Mohanraj K, de Assis LJ, Lin L, Tian C, Braus GH, Borkovich KA, Schmoll M, Larrondo LF, Samal A, Goldman GH, Benz JP (2019) Broad substrate-specific phosphorylation events are associated with the initial stage of plant cell wall recognition in Neurospora crassa. Front Microbiol 10:2317. https://doi.org/10.3389/fmicb.2019.02317
Kappel L, Munsterkotter M, Sipos G, Rodriguez CE, Gruber S (2020) Chitin and chitosan remodeling defines vegetative development and Trichoderma biocontrol. PLoS Pathog. https://doi.org/10.1371/journal.ppat.1008320
Khan RAA, Najeeb S, Hussain S, Xie B, Li Y (2020) Bioactive secondary metabolites from Trichoderma spp against phytopathogenic fungi. Microorganisms. https://doi.org/10.3390/microorganisms8060817
Khan RAA, Najeeb S, Mao Z, Ling J, Yang Y, Li Y, Xie B (2020) Bioactive secondary metabolites from Trichoderma spp against phytopathogenic bacteria and root-knot nematode. Microorganisms. https://doi.org/10.3390/microorganisms8030401
Kidwai MK, Nehra M (2017) Biotechnological applications of Trichoderma species for environmental and food security. In: Gahlawat SK, Salar RK, Siwach P, Duhan JS, Kumar S, Kaur P (eds) Plant biotechnology: recent advancements and developments. Springer, Singapore, pp 125–156
Kjaerbolling I, Vesth T, Frisvad JC, Nybo JL, Theobald S, Kildgaard S, Petersen TI, Kuo A, Sato A, Lyhne EK, Kogle ME, Wiebenga A, Kun RS, Lubbers RJM, Makela MR, Barry K, Chovatia M, Clum A, Daum C, Haridas S, He G, LaButti K, Lipzen A, Mondo S, Pangilinan J, Riley R, Salamov A, Simmons BA, Magnuson JK, Henrissat B, Mortensen UH, Larsen TO, de Vries RP, Grigoriev IV, Machida M, Baker SE, Andersen MR (2020) A comparative genomics study of 23 Aspergillus species from section Flavi. Nat Commun 11:1106. https://doi.org/10.1038/s41467-019-14051-y
Kolde R (2019) Pheatmap: pretty heatmaps. R Package Version 1:2
Koren S, Walenz BP, Berlin K, Miller JR, Bergman NH, Phillippy AM (2017) Canu: scalable and accurate long-read assembly via adaptive k-mer weighting and repeat separation. Genome Res 27:722–736. https://doi.org/10.1101/gr.215087.116
Krogh A, Larsson B, von Heijne G, Sonnhammer EL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305:567–580. https://doi.org/10.1006/jmbi.2000.4315
Kubicek CP, Herrera-Estrella A, Seidl-Seiboth V, Martinez DA, Druzhinina IS, Thon M, Zeilinger S, Casas-Flores S, Horwitz BA, Mukherjee PK, Mukherjee M, Kredics L, Alcaraz LD, Aerts A, Antal Z, Atanasova L, Cervantes-Badillo MG, Challacombe J, Chertkov O, McCluskey K, Coulpier F, Deshpande N, von Dohren H, Ebbole DJ, Esquivel-Naranjo EU, Fekete E, Flipphi M, Glaser F, Gomez-Rodriguez EY, Gruber S, Han C, Henrissat B, Hermosa R, Hernandez-Onate M, Karaffa L, Kosti I, Le Crom S, Lindquist E, Lucas S, Lubeck M, Lubeck PS, Margeot A, Metz B, Misra M, Nevalainen H, Omann M, Packer N, Perrone G, Uresti-Rivera EE, Salamov A, Schmoll M, Seiboth B, Shapiro H, Sukno S, Tamayo-Ramos JA, Tisch D, Wiest A, Wilkinson HH, Zhang M, Coutinho PM, Kenerley CM, Monte E, Baker SE, Grigoriev IV (2011) Comparative genome sequence analysis underscores mycoparasitism as the ancestral life style of Trichoderma. Genome Biol 12:R40. https://doi.org/10.1186/gb-2011-12-4-r40
Kubicek CP, Steindorff AS, Chenthamara K, Manganiello G, Henrissat B, Zhang J, Cai F, Kopchinskiy AG, Kubicek EM, Kuo A, Baroncelli R, Sarrocco S, Noronha EF, Vannacci G, Shen Q, Grigoriev IV, Druzhinina IS (2019a) Evolution and comparative genomics of the most common Trichoderma species. BMC Genomics 20:485. https://doi.org/10.1186/s12864-019-5680-7
Kubicek CP, Steindorff AS, Chenthamara K, Manganiello G, Henrissat B, Zhang J, Cai F, Kopchinskiy AG, Kubicek EM, Kuo A, Baroncelli R, Sarrocco S, Noronha EF, Vannacci G, Shen Q, Grigoriev IV, Druzhinina IS (2019b) Evolution and comparative genomics of the most common Trichoderma species. BMC Genom 20:485. https://doi.org/10.1186/s12864-019-5680-7
Kumar AG, Manisha D, Sujitha K, Peter DM, Kirubagaran R, Dharani G (2021) Genome sequence analysis of deep sea Aspergillus sydowii BOBA1 and effect of high pressure on biodegradation of spent engine oil. Sci Rep 11:9347. https://doi.org/10.1038/s41598-021-88525-9
Kurtz S, Phillippy A, Delcher AL, Smoot M, Shumway M, Antonescu C, Salzberg SL (2004) Versatile and open software for comparing large genomes. Genome Biol 5:R12. https://doi.org/10.1186/gb-2004-5-2-r12
Letunic I, Bork P (2007) Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 23:127–128. https://doi.org/10.1093/bioinformatics/btl529
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
Li H (2018) Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics 34:3094–3100. https://doi.org/10.1093/bioinformatics/bty191
Li H, Durbin R (2010) Fast and accurate long-read alignment with burrows-wheeler transform. Bioinformatics 26:589–595. https://doi.org/10.1093/bioinformatics/btp698
Li B, Walton JD (2017) Functional diversity for biomass deconstruction in family 5 subfamily 5 (GH5_5) of fungal endo-beta1,4-glucanases. Appl Microbiol Biotechnol 101:4093–4101. https://doi.org/10.1007/s00253-017-8168-x
Li WC, Huang CH, Chen CL, Chuang YC, Tung SY, Wang TF (2017) Trichoderma reesei complete genome sequence, repeat-induced point mutation, and partitioning of CAZyme gene clusters. Biotechnol Biofuels 10:170. https://doi.org/10.1186/s13068-017-0825-x
Marcais G, Delcher AL, Phillippy AM, Coston R, Salzberg SL, Zimin A (2018) MUMmer4: a fast and versatile genome alignment system. PLoS Comput Biol. https://doi.org/10.1371/journal.pcbi.1005944
Martinez D, Berka RM, Henrissat B, Saloheimo M, Arvas M, Baker SE, Chapman J, Chertkov O, Coutinho PM, Cullen D, Danchin EG, Grigoriev IV, Harris P, Jackson M, Kubicek CP, Han CS, Ho I, Larrondo LF, de Leon AL, Magnuson JK, Merino S, Misra M, Nelson B, Putnam N, Robbertse B, Salamov AA, Schmoll M, Terry A, Thayer N, Westerholm-Parvinen A, Schoch CL, Yao J, Barabote R, Nelson MA, Detter C, Bruce D, Kuske CR, Xie G, Richardson P, Rokhsar DS, Lucas SM, Rubin EM, Dunn-Coleman N, Ward M, Brettin TS (2008) Genome sequencing and analysis of the biomass-degrading fungus Trichoderma reesei (syn. Hypocrea jecorina). Nat Biotechnol 26:553–560. https://doi.org/10.1038/nbt1403
Medeiros HA, Araujo Filho JV, Freitas LG, Castillo P, Rubio MB, Hermosa R, Monte E (2017) Tomato progeny inherit resistance to the nematode Meloidogyne javanica linked to plant growth induced by the biocontrol fungus Trichoderma atroviride. Sci Rep 7:40216. https://doi.org/10.1038/srep40216
Mills RE, Walter K, Stewart C, Handsaker RE, Chen K, Alkan C, Abyzov A, Yoon SC, Ye K, Cheetham RK, Chinwalla A, Conrad DF, Fu Y, Grubert F, Hajirasouliha I, Hormozdiari F, Iakoucheva LM, Iqbal Z, Kang S, Kidd JM, Konkel MK, Korn J, Khurana E, Kural D, Lam HY, Leng J, Li R, Li Y, Lin CY, Luo R, Mu XJ, Nemesh J, Peckham HE, Rausch T, Scally A, Shi X, Stromberg MP, Stutz AM, Urban AE, Walker JA, Wu J, Zhang Y, Zhang ZD, Batzer MA, Ding L, Marth GT, McVean G, Sebat J, Snyder M, Wang J, Ye K, Eichler EE, Gerstein MB, Hurles ME, Lee C, McCarroll SA, Korbel JO, Genomes P (2011) Mapping copy number variation by population-scale genome sequencing. Nature 470:59–65. https://doi.org/10.1038/nature09708
Monclaro AV, Filho EXF (2017) Fungal lytic polysaccharide monooxygenases from family AA9: recent developments and application in lignocelullose breakdown. Int J Biol Macromol 102:771–778. https://doi.org/10.1016/j.ijbiomac.2017.04.077
Morais EM, Silva AAR, Sousa FWA, Azevedo IMB, Silva HF, Santos AMG, Junior JEAB, Carvalho CP, Eberlin MN, Porcari AM, Araujo F (2022) Endophytic Trichoderma strains isolated from forest species of the cerrado-caatinga ecotone are potential biocontrol agents against crop pathogenic fungi. PLoS ONE. https://doi.org/10.1371/journal.pone.0265824
Motta MLL, Filho JAF, de Melo RR, Zanphorlin LM, Santos CAD, de Souza AP (2021) A novel fungal metal-dependent alpha-L-arabinofuranosidase of family 54 glycoside hydrolase shows expanded substrate specificity. Sci Rep 11:10961. https://doi.org/10.1038/s41598-021-90490-2
Nagel JH, Wingfield MJ, Slippers B (2021) Increased abundance of secreted hydrolytic enzymes and secondary metabolite gene clusters define the genomes of latent plant pathogens in the Botryosphaeriaceae. BMC Genom 22:589. https://doi.org/10.1186/s12864-021-07902-w
Najjarzadeh N, Matsakas L, Rova U, Christakopoulos P (2021) How carbon source and degree of oligosaccharide polymerization affect production of cellulase-degrading enzymes by Fusarium oxysporum f. sp. lycopersici. Front Microbiol. https://doi.org/10.3389/fmicb.2021.652655
Nakkeeran S, Marimuthu T, Renukadevi P, Brindhadevi S, Jogaiah S (2021) 24 - Exploring the biogeographical diversity of Trichoderma for plant health. In: Jogaiah S (ed) Biocontrol agents and secondary metabolites. Woodhead Publishing, Sawston, pp 537–571
Okonechnikov K, Conesa A, Garcia-Alcalde F (2016) Qualimap 2: advanced multi-sample quality control for high-throughput sequencing data. Bioinformatics 32:292–294. https://doi.org/10.1093/bioinformatics/btv566
Peterson DG, Tomkins JP, Frisch DA, Wing RA, Paterson AH (2000) Construction of plant bacterial artificial chromosome (BAC) libraries: an illustrated guide. J Agri Genom 5:1–100
Priest SJ, Yadav V, Heitman J (2020) Advances in understanding the evolution of fungal genome architecture. Res. https://doi.org/10.12688/f1000research.25424.1
Ramazi S, Zahiri J (2021) Posttranslational modifications in proteins: resources, tools and prediction methods. Database. https://doi.org/10.1093/database/baab012
Rosolen RR, Aono AH, Almeida DA, Ferreira Filho JA, Horta MAC, De Souza AP (2022) Network analysis reveals different cellulose degradation strategies across Trichoderma harzianum strains associated with XYR1 and CRE1. Front Genet. https://doi.org/10.3389/fgene.2022.807243
Saravanakumar K, Li Y, Yu C, Wang QQ, Wang M, Sun J, Gao JX, Chen J (2017) Effect of Trichoderma harzianum on maize rhizosphere microbiome and biocontrol of Fusarium Stalk rot. Sci Rep 7:1771. https://doi.org/10.1038/s41598-017-01680-w
Schmoll M (2018) Regulation of plant cell wall degradation by light in Trichoderma. Fungal Biol Biotechnol 5:10. https://doi.org/10.1186/s40694-018-0052-7
Schmoll M, Dattenbock C, Carreras-Villasenor N, Mendoza-Mendoza A, Tisch D, Aleman MI, Baker SE, Brown C, Cervantes-Badillo MG, Cetz-Chel J, Cristobal-Mondragon GR, Delaye L, Esquivel-Naranjo EU, Frischmann A, Gallardo-Negrete Jde J, Garcia-Esquivel M, Gomez-Rodriguez EY, Greenwood DR, Hernandez-Onate M, Kruszewska JS, Lawry R, Mora-Montes HM, Munoz-Centeno T, Nieto-Jacobo MF, Nogueira Lopez G, Olmedo-Monfil V, Osorio-Concepcion M, Pilsyk S, Pomraning KR, Rodriguez-Iglesias A, Rosales-Saavedra MT, Sanchez-Arreguin JA, Seidl-Seiboth V, Stewart A, Uresti-Rivera EE, Wang CL, Wang TF, Zeilinger S, Casas-Flores S, Herrera-Estrella A (2016) The genomes of three uneven siblings: footprints of the lifestyles of three trichoderma species. Microbiol Mol Biol Rev 80:205–327. https://doi.org/10.1128/MMBR.00040-15
Sedlazeck FJ, Rescheneder P, Smolka M, Fang H, Nattestad M, von Haeseler A, Schatz MC (2018) Accurate detection of complex structural variations using single-molecule sequencing. Nat Methods 15:461–468. https://doi.org/10.1038/s41592-018-0001-7
Sharma S, Kour D, Rana KL, Dhiman A, Thakur S, Thakur P, Thakur S, Thakur N, Sudheer S, Yadav N, Yadav AN, Rastegari AA, Singh K (2019) Trichoderma: biodiversity, ecological significances, and industrial applications. In: Yadav AN, Mishra S, Singh S, Gupta A (eds) Recent advancement in white biotechnology through fungi diversity and enzymes perspectives. Springer International Publishing, Cham, pp 85–120
Simao FA, Waterhouse RM, Ioannidis P, Kriventseva EV, Zdobnov EM (2015) BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31:3210–3212. https://doi.org/10.1093/bioinformatics/btv351
Stanke M, Keller O, Gunduz I, Hayes A, Waack S, Morgenstern B (2006) AUGUSTUS: ab initio prediction of alternative transcripts. Nucleic Acids Res 34:W435–W439. https://doi.org/10.1093/nar/gkl200
Tatusov RL, Galperin MY, Natale DA, Koonin EV (2000) The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res 28:33–36. https://doi.org/10.1093/nar/28.1.33
Thanh VN, Thuy NT, Huong HTT, Hien DD, Hang DTM, Anh DTK, Huttner S, Larsbrink J, Olsson L (2019) Surveying of acid-tolerant thermophilic lignocellulolytic fungi in Vietnam reveals surprisingly high genetic diversity. Sci Rep 9:3674. https://doi.org/10.1038/s41598-019-40213-5
The UniProt Consortium (2021) UniProt: the universal protein knowledgebase in 2021. Nucleic Acids Res 49:D480–D489. https://doi.org/10.1093/nar/gkaa1100
Toronen P, Medlar A, Holm L (2018) PANNZER2: a rapid functional annotation web server. Nucleic Acids Res 46:W84–W88. https://doi.org/10.1093/nar/gky350
van Eerde A, Varnai A, Jameson JK, Paruch L, Moen A, Anonsen JH, Chylenski P, Steen HS, Heldal I, Bock R, Eijsink VGH, Liu-Clarke J (2020) In-depth characterization of Trichoderma reesei cellobiohydrolase TrCel7A produced in Nicotiana benthamiana reveals limitations of cellulase production in plants by host-specific post-translational modifications. Plant Biotechnol J 18:631–643. https://doi.org/10.1111/pbi.13227
Varga T, Krizsan K, Foldi C, Dima B, Sanchez-Garcia M, Sanchez-Ramirez S, Szollosi GJ, Szarkandi JG, Papp V, Albert L, Andreopoulos W, Angelini C, Antonin V, Barry KW, Bougher NL, Buchanan P, Buyck B, Bense V, Catcheside P, Chovatia M, Cooper J, Damon W, Desjardin D, Finy P, Geml J, Haridas S, Hughes K, Justo A, Karasinski D, Kautmanova I, Kiss B, Kocsube S, Kotiranta H, LaButti KM, Lechner BE, Liimatainen K, Lipzen A, Lukacs Z, Mihaltcheva S, Morgado LN, Niskanen T, Noordeloos ME, Ohm RA, Ortiz-Santana B, Ovrebo C, Racz N, Riley R, Savchenko A, Shiryaev A, Soop K, Spirin V, Szebenyi C, Tomsovsky M, Tulloss RE, Uehling J, Grigoriev IV, Vagvolgyi C, Papp T, Martin FM, Miettinen O, Hibbett DS, Nagy LG (2019) Megaphylogeny resolves global patterns of mushroom evolution. Nat Ecol Evol 3:668–678. https://doi.org/10.1038/s41559-019-0834-1
Wei H, Wu M, Fan A, Su H (2021) Recombinant protein production in the filamentous fungus Trichoderma. Chin J Chem Eng 30:74–81. https://doi.org/10.1016/j.cjche.2020.11.006
Wenger AM, Peluso P, Rowell WJ, Chang PC, Hall RJ, Concepcion GT, Ebler J, Fungtammasan A, Kolesnikov A, Olson ND, Topfer A, Alonge M, Mahmoud M, Qian Y, Chin CS, Phillippy AM, Schatz MC, Myers G, DePristo MA, Ruan J, Marschall T, Sedlazeck FJ, Zook JM, Li H, Koren S, Carroll A, Rank DR, Hunkapiller MW (2019) Accurate circular consensus long-read sequencing improves variant detection and assembly of a human genome. Nat Biotechnol 37:1155–1162. https://doi.org/10.1038/s41587-019-0217-9
Wu L, McCluskey K, Desmeth P, Liu S, Hideaki S, Yin Y, Moriya O, Itoh T, Kim CY, Lee JS, Zhou Y, Kawasaki H, Hazbon MH, Robert V, Boekhout T, Lima N, Evtushenko L, Boundy-Mills K, Bunk B, Moore ERB, Eurwilaichitr L, Ingsriswang S, Shah H, Yao S, Jin T, Huang J, Shi W, Sun Q, Fan G, Li W, Li X, Kurtboke I, Ma J (2018) The global catalogue of microorganisms 10K type strain sequencing project: closing the genomic gaps for the validly published prokaryotic and fungi species. Gigascience. https://doi.org/10.1093/gigascience/giy026
Xie BB, Qin QL, Shi M, Chen LL, Shu YL, Luo Y, Wang XW, Rong JC, Gong ZT, Li D, Sun CY, Liu GM, Dong XW, Pang XH, Huang F, Liu W, Chen XL, Zhou BC, Zhang YZ, Song XY (2014) Comparative genomics provide insights into evolution of trichoderma nutrition style. Genome Biol Evol 6:379–390. https://doi.org/10.1093/gbe/evu018
Zhang H, Yohe T, Huang L, Entwistle S, Wu P, Yang Z, Busk PK, Xu Y, Yin Y (2018) dbCAN2: a meta server for automated carbohydrate-active enzyme annotation. Nucleic Acids Res 46:W95–W101. https://doi.org/10.1093/nar/gky418
Zhang Y, Yang J, Luo L, Wang E, Wang R, Liu L, Liu J, Yuan H (2020) Low-cost cellulase-hemicellulase mixture secreted by Trichoderma harzianum EM0925 with complete saccharification efficacy of lignocellulose. Int J Mol Sci 21:371. https://doi.org/10.3390/ijms21020371
Zin NA, Badaluddin NA (2020) Biological functions of Trichoderma spp. for agriculture applications. Ann Agric Sci 65:168–178. https://doi.org/10.1016/j.aoas.2020.09.003
Acknowledgements
We are grateful to CBMAI Campinas and SP for conceiving the fungal isolates used in the current study; the Center of Molecular Biology and Genetic Engineering (CBMEG) at the University of Campinas and SP for the use of the center and laboratory space; and the São Paulo Research Foundation (FAPESP), the Coordination of Improvement of Higher Education Personnel (CAPES, Computational Biology Program), and the Brazilian National Council for Technological and Scientific Development (CNPq) for supporting the project and researchers.
Funding
Financial support for this work was provided by the São Paulo Research Foundation (FAPESP—Process number 2015/09202-0 and 2018/19660-4) and the Coordination for the Improvement of Higher Education Personnel (CAPES, Computational Biology Program—Process number 88882.160095/2013-01). RRR received a PhD fellowship from CAPES (88887.482201/2020-00) and FAPESP (2020/13420-1), PHCA received a PhD fellowship from CAPES (88887.612254/2021–00), MACH received a postdoctoral fellowship from FAPESP (2020/10536-9), and APS received a research fellowship from the Brazilian National Council for Technological and Scientific Development (CNPq- Process number 312777/2018-3).
Author information
Authors and Affiliations
Contributions
RRR: writing—original draft, methodology, formal analysis, and visualization. MACH: conceptualization, methodology, and writing—review & editing. PHCA: methodology and resources. CCS: methodology and formal analysis. DAS: methodology and resources. GHG: writing—review & editing. APS: conceptualization, supervision, review & editing, and funding acquisition.
Corresponding author
Ethics declarations
Conflict of interests
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as potential conflict of interests.
Ethics approval
Not applicable.
Informed consent
Not applicable.
Additional information
Communicated by Martine Collart.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Rosolen, R.R., Horta, M.A.C., de Azevedo, P.H.C. et al. Whole-genome sequencing and comparative genomic analysis of potential biotechnological strains of Trichoderma harzianum, Trichoderma atroviride, and Trichoderma reesei. Mol Genet Genomics 298, 735–754 (2023). https://doi.org/10.1007/s00438-023-02013-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00438-023-02013-5