Argonaute and Dicer are essential for communication between Trichoderma atroviride and fungal hosts during mycoparasitism

Enriquez-Felix, Eli Efrain; Pérez-Salazar, Camilo; Rico-Ruiz, José Guillermo; Calheiros de Carvalho, Ana; Cruz-Morales, Pablo; Villalobos-Escobedo, José Manuel; Herrera-Estrella, Alfredo; Goldman, ed., Gustavo H.; Donofrio, Nicole

doi:10.1128/spectrum.03165-23

Title: Argonaute and Dicer are essential for communication between Trichoderma atroviride and fungal hosts during mycoparasitism

Journal Article · 01 April 2024 · Microbiology Spectrum

DOI: https://doi.org/10.1128/spectrum.03165-23 · OSTI ID:2318759

Enriquez-Felix, Eli Efrain ^[1]; Pérez-Salazar, Camilo ^[1]; Rico-Ruiz, José Guillermo ^[1]; Calheiros de Carvalho, Ana ^[2]; Cruz-Morales, Pablo ^[3];

^[4];

^[5]; Goldman, ed., Gustavo H.; Donofrio, Nicole

Laboratorio Nacional de Genómica para la Biodiversidad-Unidad de Genómica Avanzada, Cinvestav Campus Guanajuato, Irapuato, Guanajuato, Mexico
Novo Nordisk Center for Biosustainability, Technical University of Denmark, Lyngby, Denmark
Novo Nordisk Center for Biosustainability, Technical University of Denmark, Lyngby, Denmark, The LatAmBio Initiative, Irapuato, Guanajuato, Mexico
Laboratorio Nacional de Genómica para la Biodiversidad-Unidad de Genómica Avanzada, Cinvestav Campus Guanajuato, Irapuato, Guanajuato, Mexico, The LatAmBio Initiative, Irapuato, Guanajuato, Mexico, Plant and Microbial Biology Department, University of California, Berkeley, Carlifornia, USA, Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, Carlifornia, USA
Laboratorio Nacional de Genómica para la Biodiversidad-Unidad de Genómica Avanzada, Cinvestav Campus Guanajuato, Irapuato, Guanajuato, Mexico, The LatAmBio Initiative, Irapuato, Guanajuato, Mexico

ABSTRACT Trichoderma species are known for their mycoparasitic activity against phytopathogenic fungi that cause significant economic losses in agriculture. During mycoparasitism, Trichoderma spp. recognize molecules produced by the host fungus and release secondary metabolites and hydrolytic enzymes to kill and degrade the host’s cell wall. Here, we explored the participation of the Trichoderma atroviride RNAi machinery in the interaction with six phytopathogenic fungi of economic importance. We determined that both Argonaute-3 and Dicer-2 play an essential role during mycoparasitism. Using an RNA-Seq approach, we identified that perception, detox, and cell wall degradation depend on the T. atroviride -RNAi when interacting with Alternaria alternata, Rhizoctonia solani AG2 , and R. solani AG5. Furthermore, we constructed a gene co-expression network that provides evidence of two gene modules regulated by RNAi, which play crucial roles in essential processes during mycoparasitism. In addition, based on small RNA-seq, we conclude that siRNAs regulate amino acid and carbon metabolism and communication during the Trichoderma -host interaction. Interestingly, our data suggest that siRNAs might regulate allorecognition ( het ) and transport genes in a cross-species manner. Thus, these results reveal a fine-tuned regulation in T. atroviride dependent on siRNAs that is essential during the biocontrol of phytopathogenic fungi, showing a greater complexity of this process than previously established. IMPORTANCE There is an increasing need for plant disease control without chemical pesticides to avoid environmental pollution and resistance, and the health risks associated with the application of pesticides are increasing. Employing Trichoderma species in agriculture to control fungal diseases is an alternative plant protection strategy that overcomes these issues without utilizing chemical fungicides. Therefore, understanding the biocontrol mechanisms used by Trichoderma species to antagonize other fungi is critical. Although there has been extensive research about the mechanisms involved in the mycoparasitic capability of Trichoderma species, there are still unsolved questions related to how Trichoderma regulates recognition, attack, and defense mechanisms during interaction with a fungal host. In this work, we report that the Argonaute and Dicer components of the RNAi machinery and the small RNAs they process are essential for gene regulation during mycoparasitism by Trichoderma atroviride .

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Sponsoring Organization:: USDOE

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 2318759

Alternate ID(s):: OSTI ID: 2318771

Journal Information:: Microbiology Spectrum, Journal Name: Microbiology Spectrum Journal Issue: 4 Vol. 12; ISSN 2165-0497

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

References (72)

HISAT: a fast spliced aligner with low memory requirements Kim, Daehwan; Langmead, Ben; Salzberg, Steven L. Nature Methods, Vol. 12, Issue 4 https://doi.org/10.1038/nmeth.3317	journal	March 2015
miRNA Target Prediction in Plants Fahlgren, Noah; Carrington, James C. Methods in Molecular Biology https://doi.org/10.1007/978-1-60327-005-2_4	book	January 2009
Dicer and Argonaute Genes Involved in RNA Interference in the Entomopathogenic Fungus Metarhizium robertsii Meng, Huimin; Wang, Zhangxun; Wang, Yulong Applied and Environmental Microbiology, Vol. 83, Issue 7 https://doi.org/10.1128/AEM.03230-16	journal	April 2017
BlastKOALA and GhostKOALA: KEGG Tools for Functional Characterization of Genome and Metagenome Sequences Kanehisa, Minoru; Sato, Yoko; Morishima, Kanae Journal of Molecular Biology, Vol. 428, Issue 4 https://doi.org/10.1016/j.jmb.2015.11.006	journal	February 2016
Trichoderma: the genomics of opportunistic success Druzhinina, Irina S.; Seidl-Seiboth, Verena; Herrera-Estrella, Alfredo Nature Reviews Microbiology, Vol. 9, Issue 10 https://doi.org/10.1038/nrmicro2637	journal	September 2011
The RNAi machinery regulates growth and development in the filamentous fungus Trichoderma atroviride: Function of sRNAs in Trichoderma Carreras-Villaseñor, Nohemi; Esquivel-Naranjo, Edgardo U.; Villalobos-Escobedo, J. Manuel Molecular Microbiology, Vol. 89, Issue 1 https://doi.org/10.1111/mmi.12261	journal	June 2013
Quelling: transient inactivation of gene expression in Neurospora crassa by transformation with homologous sequences Romano, Nicoletta; Macino, Giuseppe Molecular Microbiology, Vol. 6, Issue 22 https://doi.org/10.1111/j.1365-2958.1992.tb02202.x	journal	November 1992
Candida albicans Sun41p, a Putative Glycosidase, Is Involved in Morphogenesis, Cell Wall Biogenesis, and Biofilm Formation Hiller, Ekkehard; Heine, Sonja; Brunner, Herwig Eukaryotic Cell, Vol. 6, Issue 11 https://doi.org/10.1128/EC.00285-07	journal	November 2007
Fungal secondary metabolism: regulation, function and drug discovery Keller, Nancy P. Nature Reviews Microbiology, Vol. 17, Issue 3 https://doi.org/10.1038/s41579-018-0121-1	journal	December 2018
miRDeep2 accurately identifies known and hundreds of novel microRNA genes in seven animal clades Friedländer, Marc R.; Mackowiak, Sebastian D.; Li, Na Nucleic Acids Research, Vol. 40, Issue 1 https://doi.org/10.1093/nar/gkr688	journal	September 2011
Comprehensive re-analysis of hairpin small RNAs in fungi reveals loci with conserved links Johnson, Nathan R.; Larrondo, Luis F.; Álvarez, José M. eLife, Vol. 11 https://doi.org/10.7554/eLife.83691	journal	December 2022
Evolution and Diversification of RNA Silencing Proteins in Fungi Nakayashiki, Hitoshi; Kadotani, Naoki; Mayama, Shigeyuki Journal of Molecular Evolution, Vol. 63, Issue 1 https://doi.org/10.1007/s00239-005-0257-2	journal	June 2006
The Nag1 N-acetylglucosaminidase of Trichoderma atroviride is essential for chitinase induction by chitin and of major relevance to biocontrol Zeilinger, Susanne; Brunner, Kurt; Peterbauer, Clemens K. Current Genetics, Vol. 43, Issue 4 https://doi.org/10.1007/s00294-003-0399-y	journal	July 2003
The Epl1 and Sm1 proteins from Trichoderma atroviride and Trichoderma virens differentially modulate systemic disease resistance against different life style pathogens in Solanum lycopersicum Salas-Marina, Miguel A.; Isordia-Jasso, MarÃa I.; Islas-Osuna, MarÃa A. Frontiers in Plant Science, Vol. 6 https://doi.org/10.3389/fpls.2015.00077	journal	February 2015
The mycoparasitic fungus Clonostachys rosea responds with both common and specific gene expression during interspecific interactions with fungal prey Nygren, Kristiina; Dubey, Mukesh; Zapparata, Antonio Evolutionary Applications, Vol. 11, Issue 6 https://doi.org/10.1111/eva.12609	journal	March 2018
limma powers differential expression analyses for RNA-sequencing and microarray studies Ritchie, Matthew E.; Phipson, Belinda; Wu, Di Nucleic Acids Research, Vol. 43, Issue 7 https://doi.org/10.1093/nar/gkv007	journal	January 2015
Mutants defective in a Mucor circinelloides dicer-like gene are not compromised in siRNA silencing but display developmental defects Nicolás, Francisco E.; de Haro, Juan P.; Torres-Martínez, Santiago Fungal Genetics and Biology, Vol. 44, Issue 6 https://doi.org/10.1016/j.fgb.2006.09.003	journal	June 2007
RNA and transcriptional modulation of gene expression Hawkins, Peter G.; Morris, Kevin V. Cell Cycle, Vol. 7, Issue 5 https://doi.org/10.4161/cc.7.5.5522	journal	March 2008
rco-3 , a Gene Involved in Glucose Transport and Conidiation in Neurospora crassa Madi, Lea; McBride, Sheila A.; Bailey, Lori A. Genetics, Vol. 146, Issue 2 https://doi.org/10.1093/genetics/146.2.499	journal	June 1997
The R package Rsubread is easier, faster, cheaper and better for alignment and quantification of RNA sequencing reads Liao, Yang; Smyth, Gordon K.; Shi, Wei Nucleic Acids Research, Vol. 47, Issue 8 https://doi.org/10.1093/nar/gkz114	journal	February 2019
psRNATarget: a plant small RNA target analysis server (2017 release) Dai, Xinbin; Zhuang, Zhaohong; Zhao, Patrick Xuechun Nucleic Acids Research, Vol. 46, Issue W1 https://doi.org/10.1093/nar/gky316	journal	April 2018
ShortStack: Comprehensive annotation and quantification of small RNA genes Axtell, M. J. RNA, Vol. 19, Issue 6 https://doi.org/10.1261/rna.035279.112	journal	April 2013
Bioactive Secondary Metabolites from Trichoderma spp. against Phytopathogenic Bacteria and Root-Knot Nematode Khan, Raja Asad Ali; Najeeb, Saba; Mao, Zhenchuan Microorganisms, Vol. 8, Issue 3 https://doi.org/10.3390/microorganisms8030401	journal	March 2020
Identification of Mycoparasitism-Related Genes in Trichoderma atroviride Reithner, Barbara; Ibarra-Laclette, Enrique; Mach, Robert L. Applied and Environmental Microbiology, Vol. 77, Issue 13 https://doi.org/10.1128/AEM.00129-11	journal	July 2011
Identification of Mycoparasitism-Related Genes against the Phytopathogen Botrytis cinerea via Transcriptome Analysis of Trichoderma harzianum T4 Wang, Yaping; Zhu, Xiaochong; Wang, Jian Journal of Fungi, Vol. 9, Issue 3 https://doi.org/10.3390/jof9030324	journal	March 2023
Molecular dialogues between Trichoderma and roots: Role of the fungal secretome Mendoza-Mendoza, Artemio; Zaid, Rinat; Lawry, Robert Fungal Biology Reviews, Vol. 32, Issue 2 https://doi.org/10.1016/j.fbr.2017.12.001	journal	March 2018
Enhanced Plant Immunity Using Trichoderma Contreras-Cornejo, Hexon Angel; Macías-Rodríguez, Lourdes; López-Bucio, Jesús Salvador Biotechnology and Biology of Trichoderma https://doi.org/10.1016/B978-0-444-59576-8.00036-9	book	February 2014
InterPro in 2022 Paysan-Lafosse, Typhaine; Blum, Matthias; Chuguransky, Sara Nucleic Acids Research, Vol. 51, Issue D1 https://doi.org/10.1093/nar/gkac993	journal	November 2022
Efflux in Fungi: La Pièce de Résistance Coleman, Jeffrey J.; Mylonakis, Eleftherios PLoS Pathogens, Vol. 5, Issue 6 https://doi.org/10.1371/journal.ppat.1000486	journal	June 2009
Trichoderma atroviride hyphal regeneration and conidiation depend on cell-signaling processes regulated by a microRNA-like RNA Villalobos-Escobedo, José M.; Martínez-Hernández, J. Pedro; Pelagio-Flores, Ramón Microbial Genomics, Vol. 8, Issue 10 https://doi.org/10.1099/mgen.0.000869	journal	October 2022
WISH, a novel CFEM GPCR is indispensable for surface sensing, asexual and pathogenic differentiation in rice blast fungus Sabnam, Nazmiara; Roy Barman, Subhankar Fungal Genetics and Biology, Vol. 105 https://doi.org/10.1016/j.fgb.2017.05.006	journal	August 2017
RNA Interference in Fungi: Pathways, Functions, and Applications Dang, Yunkun; Yang, Qiuying; Xue, Zhihong Eukaryotic Cell, Vol. 10, Issue 9 https://doi.org/10.1128/EC.05109-11	journal	July 2011
Discovery of cyclohexadepsipeptides with anti-Zika virus activities and biosynthesis of the nonproteinogenic building block (3S)-methyl-l-proline Yuan, Bochuan; Wu, Ziwei; Ji, Wei Journal of Biological Chemistry, Vol. 297, Issue 1 https://doi.org/10.1016/j.jbc.2021.100822	journal	July 2021
Identification of a New Biocontrol Gene in Trichoderma atroviride: The Role of an ABC Transporter Membrane Pump in the Interaction with Different Plant-Pathogenic Fungi Ruocco, Michelina; Lanzuise, Stefania; Vinale, Francesco Molecular Plant-Microbe Interactions®, Vol. 22, Issue 3 https://doi.org/10.1094/MPMI-22-3-0291	journal	March 2009
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 Love, Michael I.; Huber, Wolfgang; Anders, Simon Genome Biology, Vol. 15, Issue 12 https://doi.org/10.1186/s13059-014-0550-8	journal	December 2014
Characterization of ech-42, a Trichoderma harzianum endochitinase gene expressed during mycoparasitism. Carsolio, C.; Gutiérrez, A.; Jiménez, B. Proceedings of the National Academy of Sciences, Vol. 91, Issue 23 https://doi.org/10.1073/pnas.91.23.10903	journal	November 1994
Identification of microRNA-Like RNAs in the Filamentous Fungus Trichoderma reesei by Solexa Sequencing Kang, Kang; Zhong, Jiasheng; Jiang, Liang PLoS ONE, Vol. 8, Issue 10 https://doi.org/10.1371/journal.pone.0076288	journal	October 2013
Trimmomatic: a flexible trimmer for Illumina sequence data Bolger, Anthony M.; Lohse, Marc; Usadel, Bjoern Bioinformatics, Vol. 30, Issue 15 https://doi.org/10.1093/bioinformatics/btu170	journal	April 2014
Role of Dicer-Dependent RNA Interference in Regulating Mycoparasitic Interactions Piombo, Edoardo; Vetukuri, Ramesh R.; Broberg, Anders Microbiology Spectrum, Vol. 9, Issue 2 https://doi.org/10.1128/Spectrum.01099-21	journal	October 2021
Identification of effector-like proteins in Trichoderma spp. and role of a hydrophobin in the plant-fungus interaction and mycoparasitism Guzmán-Guzmán, Paulina; Alemán-Duarte, Mario Iván; Delaye, Luis BMC Genetics, Vol. 18, Issue 1 https://doi.org/10.1186/s12863-017-0481-y	journal	February 2017
Comparative Analysis of Secretome Profiles of Manganese(II)-Oxidizing Ascomycete Fungi Zeiner, Carolyn A.; Purvine, Samuel O.; Zink, Erika M. PLOS ONE, Vol. 11, Issue 7 https://doi.org/10.1371/journal.pone.0157844	journal	July 2016
Transcriptomic response of the mycoparasitic fungus Trichoderma atroviride to the presence of a fungal prey Seidl, Verena; Song, Lifu; Lindquist, Erika BMC Genomics, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2164-10-567	journal	January 2009
Analysis of the Properties of 44 ABC Transporter Genes from Biocontrol Agent Trichoderma asperellum ACCC30536 and Their Responses to Pathogenic Alternaria alternata Toxin Stress Du, Hua-Ying; Zhang, Yu-Zhou; Liu, Kuo Current Issues in Molecular Biology, Vol. 45, Issue 2 https://doi.org/10.3390/cimb45020101	journal	February 2023
edgeR: a Bioconductor package for differential expression analysis of digital gene expression data Robinson, M. D.; McCarthy, D. J.; Smyth, G. K. Bioinformatics, Vol. 26, Issue 1 https://doi.org/10.1093/bioinformatics/btp616	journal	November 2009
TAPIR, a web server for the prediction of plant microRNA targets, including target mimics Bonnet, Eric; He, Ying; Billiau, Kenny Bioinformatics, Vol. 26, Issue 12 https://doi.org/10.1093/bioinformatics/btq233	journal	April 2010
Origins and Mechanisms of miRNAs and siRNAs Carthew, Richard W.; Sontheimer, Erik J. Cell, Vol. 136, Issue 4 https://doi.org/10.1016/j.cell.2009.01.035	journal	February 2009
Cutadapt removes adapter sequences from high-throughput sequencing reads Martin, Marcel EMBnet.journal, Vol. 17, Issue 1 https://doi.org/10.14806/ej.17.1.200	journal	May 2011
Trichoderma Species: Versatile Plant Symbionts Guzmán-Guzmán, Paulina; Porras-Troncoso, María Daniela; Olmedo-Monfil, Vianey Phytopathology®, Vol. 109, Issue 1 https://doi.org/10.1094/PHYTO-07-18-0218-RVW	journal	January 2019
Different Components of the RNA Interference Machinery Are Required for Conidiation, Ascosporogenesis, Virulence, Deoxynivalenol Production, and Fungal Inhibition by Exogenous Double-Stranded RNA in the Head Blight Pathogen Fusarium graminearum Gaffar, Fatima Yousif; Imani, Jafargholi; Karlovsky, Petr Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.01662	journal	August 2019
Trichoderma harzianum expressed sequence tags for identification of genes with putative roles in mycoparasitism against Fusarium solani Steindorff, Andrei Stecca; Silva, Roberto do Nascimento; Coelho, Alexandre Siqueira Guedes Biological Control, Vol. 61, Issue 2 https://doi.org/10.1016/j.biocontrol.2012.01.014	journal	May 2012
A putative catabolite-repressed cell wall protein from the mycoparasitic fungus Trichoderma harzianum Lora, José M.; de la Cruz, Jésus; Benítez, Tahía Molecular and General Genetics MGG, Vol. 242, Issue 4 https://doi.org/10.1007/BF00281797	journal	February 1994
Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks Shannon, P. Genome Research, Vol. 13, Issue 11 https://doi.org/10.1101/gr.1239303	journal	November 2003
Comparative transcriptomics reveals different strategies of Trichoderma mycoparasitism Atanasova, Lea; Crom, Stephane Le; Gruber, Sabine BMC Genomics, Vol. 14, Issue 1 https://doi.org/10.1186/1471-2164-14-121	journal	January 2013
A Single Argonaute Gene Participates in Exogenous and Endogenous RNAi and Controls Cellular Functions in the Basal Fungus Mucor circinelloides Cervantes, María; Vila, Ana; Nicolás, Francisco E. PLoS ONE, Vol. 8, Issue 7 https://doi.org/10.1371/journal.pone.0069283	journal	July 2013
Comprehensive analysis of microRNA-Seq and target mRNAs of rice sheath blight pathogen provides new insights into pathogenic regulatory mechanisms Lin, Runmao; He, Liye; He, Jiayu DNA Research, Vol. 23, Issue 5 https://doi.org/10.1093/dnares/dsw024	journal	July 2016
Ultrafast and memory-efficient alignment of short DNA sequences to the human genome Langmead, Ben; Trapnell, Cole; Pop, Mihai Genome Biology, Vol. 10, Issue 3 https://doi.org/10.1186/gb-2009-10-3-r25	journal	January 2009
Enzyme Diffusion from Trichoderma atroviride (= T. harzianum P1) to Rhizoctonia solani Is a Prerequisite for Triggering of Trichoderma ech42 Gene Expression before Mycoparasitic Contact Kullnig, Cornelia; Mach, Robert L.; Lorito, Matteo Applied and Environmental Microbiology, Vol. 66, Issue 5 https://doi.org/10.1128/AEM.66.5.2232-2234.2000	journal	May 2000
antiSMASH 7.0: new and improved predictions for detection, regulation, chemical structures and visualisation Blin, Kai; Shaw, Simon; Augustijn, Hannah E. Nucleic Acids Research, Vol. 51, Issue W1 https://doi.org/10.1093/nar/gkad344	journal	May 2023
WGCNA: an R package for weighted correlation network analysis Langfelder, Peter; Horvath, Steve BMC Bioinformatics, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2105-9-559	journal	December 2008
Falco: high-speed FastQC emulation for quality control of sequencing data de Sena Brandine, Guilherme; Smith, Andrew D. F1000Research, Vol. 8 https://doi.org/10.12688/f1000research.21142.2	journal	January 2019
Rfam 14: expanded coverage of metagenomic, viral and microRNA families Kalvari, Ioanna; Nawrocki, Eric P.; Ontiveros-Palacios, Nancy Nucleic Acids Research, Vol. 49, Issue D1 https://doi.org/10.1093/nar/gkaa1047	journal	November 2020
A fungal pathogen deploys a small silencing RNA that attenuates mosquito immunity and facilitates infection Cui, Chunlai; Wang, Yan; Liu, Jingnan Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-12323-1	journal	September 2019
Small RNA Functions Are Required for Growth and Development of Magnaporthe oryzae Raman, Vidhyavathi; Simon, Stacey A.; Demirci, Feray Molecular Plant-Microbe Interactions®, Vol. 30, Issue 7 https://doi.org/10.1094/MPMI-11-16-0236-R	journal	July 2017
Multiple environmental signals determine the transcriptional activation of the mycoparasitism related gene prb1 in Trichoderma atroviride Olmedo-Monfil, V.; Mendoza-Mendoza, A.; Gómez, I. Molecular Genetics and Genomics, Vol. 267, Issue 6 https://doi.org/10.1007/s00438-002-0703-4	journal	August 2002
Improved scoring of functional groups from gene expression data by decorrelating GO graph structure Alexa, A.; Rahnenfuhrer, J.; Lengauer, T. Bioinformatics, Vol. 22, Issue 13 https://doi.org/10.1093/bioinformatics/btl140	journal	April 2006
Identification of differentially expressed genes from Trichoderma harzianum during growth on cell wall of Fusarium solani as a tool for biotechnological application Vieira, Pabline Marinho; Coelho, Alexandre Siqueira Guedes; Steindorff, Andrei Stecca BMC Genomics, Vol. 14, Issue 1 https://doi.org/10.1186/1471-2164-14-177	journal	January 2013
Insecticidal Cyclodepsipeptides from Beauveria felina Langenfeld, Aude; Blond, Alain; Gueye, Sabelle Journal of Natural Products, Vol. 74, Issue 4 https://doi.org/10.1021/np100890n	journal	March 2011
Fungal Small RNAs Suppress Plant Immunity by Hijacking Host RNA Interference Pathways Weiberg, Arne; Wang, Ming; Lin, Feng-Mao Science, Vol. 342, Issue 6154 https://doi.org/10.1126/science.1239705	journal	October 2013
Comparative genome sequence analysis underscores mycoparasitism as the ancestral life style of Trichoderma Kubicek, Christian P.; Herrera-Estrella, Alfredo; Seidl-Seiboth, Verena Genome Biology, Vol. 12, Issue 4 https://doi.org/10.1186/gb-2011-12-4-r40	journal	April 2011
The expression of genes involved in parasitism by Trichoderma harzianum is triggered by a diffusible factor Cortés, C.; Gutiérrez, A.; Olmedo, V. Molecular and General Genetics MGG, Vol. 260, Issue 2-3 https://doi.org/10.1007/s004380050889	journal	November 1998
RNAi-Related Dicer and Argonaute Proteins Play Critical Roles for Meiocyte Formation, Chromosome-Axes Lengths and Crossover Patterning in the Fungus Sordaria macrospora Girard, Chloe; Budin, Karine; Boisnard, Stéphanie Frontiers in Cell and Developmental Biology, Vol. 9 https://doi.org/10.3389/fcell.2021.684108	journal	June 2021
Improved biocontrol activity of Trichoderma harzianum by over-expression of the proteinase-encoding gene prb1 Flores, A.; Chet, I.; Herrera-Estrella, A. Current Genetics, Vol. 31, Issue 1 https://doi.org/10.1007/s002940050173	journal	January 1997

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