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Title: Several steps of lateral gene transfer followed by events of ‘birth-and-death’ evolution shaped a fungal sorbicillinoid biosynthetic gene cluster

Abstract

Background: Sorbicillinoids are a family of complex cyclic polyketides produced by only a small number of distantly related ascomycete fungi such as Trichoderma (Sordariomycetes) and Penicillium (Eurotiomycetes). In T. reesei, they are synthesized by a gene cluster consisting of eight genes including two polyketide synthases (PKS). To reconstruct the evolutionary origin of this gene cluster, we examined the occurrence of these eight genes in ascomycetes. Results: A cluster comprising at least six of them was only found in Hypocreales (Acremonium chrysogenum, Ustilaginoidea virens, Trichoderma species from section Longibrachiatum) and in Penicillium rubens (Eurotiales). In addition, Colletotrichum graminicola contained the two pks (sor1 and sor2), but not the other sor genes. A. chrysogenum was the evolutionary eldest species in which sor1, sor2, sor3, sor4 and sor6 were present. Sor5 was gained by lateral gene transfer (LGT) from P. rubens. In the younger Hypocreales (U. virens, Trichoderma spp.), the cluster evolved by vertical transfer, but sor2 was lost and regained by LGT from C. graminicola. SorB (=sor2) and sorD (=sor4) were symplesiomorphic in P. rubens, whereas sorA, sorC and sorF were obtained by LGT from A. chrysogenum, and sorE by LGT from Pestalotiopsis fici (Xylariales). The sorbicillinoid gene cluster in Trichoderma sectionmore » Longibrachiatum is under strong purifying selection. The T. reesei sor genes are expressed during fast vegetative growth, during antagonism of other fungi and regulated by the secondary metabolism regulator LAE1. Conclusions: Our findings pinpoint the evolution of the fungal sorbicillinoid biosynthesis gene cluster. The core cluster arose in early Hypocreales, and was complemented by LGT. During further speciation in the Hypocreales, it became subject to birth and death evolution in selected lineages. In P. rubrens (Eurotiales), two cluster genes were symplesiomorphic, and the whole cluster formed by LGT from at least two different fungal donors.« less

Authors:
 [1];  [1];  [1]
  1. Technische Univ. Wien (Austria). Inst. of Chemical Engineering. Research Area Biochemical Technology. Microbiology Group
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division
OSTI Identifier:
1626780
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
BMC Evolutionary Biology (Online)
Additional Journal Information:
Journal Name: BMC Evolutionary Biology (Online); Journal Volume: 16; Journal Issue: 1; Journal ID: ISSN 1471-2148
Publisher:
BioMed Central
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Evolutionary Biology; Genetics & Heredity; Trichoderma; Penicillium; Lateral gene transfer; Secondary metabolites; Birth-and-death evolution; PKS

Citation Formats

Druzhinina, Irina S., Kubicek, Eva M., and Kubicek, Christian P. Several steps of lateral gene transfer followed by events of ‘birth-and-death’ evolution shaped a fungal sorbicillinoid biosynthetic gene cluster. United States: N. p., 2016. Web. doi:10.1186/s12862-016-0834-6.
Druzhinina, Irina S., Kubicek, Eva M., & Kubicek, Christian P. Several steps of lateral gene transfer followed by events of ‘birth-and-death’ evolution shaped a fungal sorbicillinoid biosynthetic gene cluster. United States. https://doi.org/10.1186/s12862-016-0834-6
Druzhinina, Irina S., Kubicek, Eva M., and Kubicek, Christian P. Thu . "Several steps of lateral gene transfer followed by events of ‘birth-and-death’ evolution shaped a fungal sorbicillinoid biosynthetic gene cluster". United States. https://doi.org/10.1186/s12862-016-0834-6. https://www.osti.gov/servlets/purl/1626780.
@article{osti_1626780,
title = {Several steps of lateral gene transfer followed by events of ‘birth-and-death’ evolution shaped a fungal sorbicillinoid biosynthetic gene cluster},
author = {Druzhinina, Irina S. and Kubicek, Eva M. and Kubicek, Christian P.},
abstractNote = {Background: Sorbicillinoids are a family of complex cyclic polyketides produced by only a small number of distantly related ascomycete fungi such as Trichoderma (Sordariomycetes) and Penicillium (Eurotiomycetes). In T. reesei, they are synthesized by a gene cluster consisting of eight genes including two polyketide synthases (PKS). To reconstruct the evolutionary origin of this gene cluster, we examined the occurrence of these eight genes in ascomycetes. Results: A cluster comprising at least six of them was only found in Hypocreales (Acremonium chrysogenum, Ustilaginoidea virens, Trichoderma species from section Longibrachiatum) and in Penicillium rubens (Eurotiales). In addition, Colletotrichum graminicola contained the two pks (sor1 and sor2), but not the other sor genes. A. chrysogenum was the evolutionary eldest species in which sor1, sor2, sor3, sor4 and sor6 were present. Sor5 was gained by lateral gene transfer (LGT) from P. rubens. In the younger Hypocreales (U. virens, Trichoderma spp.), the cluster evolved by vertical transfer, but sor2 was lost and regained by LGT from C. graminicola. SorB (=sor2) and sorD (=sor4) were symplesiomorphic in P. rubens, whereas sorA, sorC and sorF were obtained by LGT from A. chrysogenum, and sorE by LGT from Pestalotiopsis fici (Xylariales). The sorbicillinoid gene cluster in Trichoderma section Longibrachiatum is under strong purifying selection. The T. reesei sor genes are expressed during fast vegetative growth, during antagonism of other fungi and regulated by the secondary metabolism regulator LAE1. Conclusions: Our findings pinpoint the evolution of the fungal sorbicillinoid biosynthesis gene cluster. The core cluster arose in early Hypocreales, and was complemented by LGT. During further speciation in the Hypocreales, it became subject to birth and death evolution in selected lineages. In P. rubrens (Eurotiales), two cluster genes were symplesiomorphic, and the whole cluster formed by LGT from at least two different fungal donors.},
doi = {10.1186/s12862-016-0834-6},
journal = {BMC Evolutionary Biology (Online)},
number = 1,
volume = 16,
place = {United States},
year = {Thu Dec 01 00:00:00 EST 2016},
month = {Thu Dec 01 00:00:00 EST 2016}
}

Works referenced in this record:

Systems Analysis of Lactose Metabolism in Trichoderma reesei Identifies a Lactose Permease That Is Essential for Cellulase Induction
journal, May 2013


Comparison of phylogenetic trees
journal, February 1981


Molecular phylogeny and species delimitation in the section Longibrachiatum of Trichoderma
journal, May 2012

  • Druzhinina, Irina S.; Komoń-Zelazowska, Monika; Ismaiel, Adnan
  • Fungal Genetics and Biology, Vol. 49, Issue 5, p. 358-368
  • DOI: 10.1016/j.fgb.2012.02.004

Multiple GAL pathway gene clusters evolved independently and by different mechanisms in fungi
journal, May 2010

  • Slot, J. C.; Rokas, A.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 22
  • DOI: 10.1073/pnas.0914418107

TOPALi: software for automatic identification of recombinant sequences within DNA multiple alignments
journal, February 2004


New Algorithms and Methods to Estimate Maximum-Likelihood Phylogenies: Assessing the Performance of PhyML 3.0
journal, March 2010

  • Guindon, Stéphane; Dufayard, Jean-François; Lefort, Vincent
  • Systematic Biology, Vol. 59, Issue 3
  • DOI: 10.1093/sysbio/syq010

Sorbicillin Analogues and Related Dimeric Compounds from Penicillium n otatum
journal, June 2005

  • Maskey, Rajendra P.; Grün-Wollny, Iris; Laatsch, Hartmut
  • Journal of Natural Products, Vol. 68, Issue 6
  • DOI: 10.1021/np040137t

Ancient Horizontal Gene Transfer from Bacteria Enhances Biosynthetic Capabilities of Fungi
journal, February 2009


A mycorrhizae-like gene regulates stem cell and gametophore development in mosses
journal, April 2020


Multiple recent horizontal transfers of a large genomic region in cheese making fungi
journal, January 2014

  • Cheeseman, Kevin; Ropars, Jeanne; Renault, Pierre
  • Nature Communications, Vol. 5, Issue 1
  • DOI: 10.1038/ncomms3876

Horizontal Transfer of a Large and Highly Toxic Secondary Metabolic Gene Cluster between Fungi
journal, January 2011


CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice
journal, January 1994

  • Thompson, Julie D.; Higgins, Desmond G.; Gibson, Toby J.
  • Nucleic Acids Research, Vol. 22, Issue 22, p. 4673-4680
  • DOI: 10.1093/nar/22.22.4673

Widespread impact of horizontal gene transfer on plant colonization of land
journal, January 2012

  • Yue, Jipei; Hu, Xiangyang; Sun, Hang
  • Nature Communications, Vol. 3, Issue 1
  • DOI: 10.1038/ncomms2148

Gene transfer into the fungi
journal, July 2011

  • Richards, Thomas A.; Leonard, Guy; Soanes, Darren M.
  • Fungal Biology Reviews, Vol. 25, Issue 2
  • DOI: 10.1016/j.fbr.2011.04.003

The metabolites of Trichoderma longibrachiatum . Part 1. Isolation of the metabolites and the structure of trichodimerol
journal, October 1992

  • Andrade, Romano; Ayer, William A.; Mebe, Paul P.
  • Canadian Journal of Chemistry, Vol. 70, Issue 10
  • DOI: 10.1139/v92-320

Genome Sequence and Annotation of Trichoderma parareesei , the Ancestor of the Cellulase Producer Trichoderma reesei
journal, August 2015

  • Yang, Dongqing; Pomraning, Kyle; Kopchinskiy, Alexey
  • Genome Announcements, Vol. 3, Issue 4
  • DOI: 10.1128/genomeA.00885-15

Phylogenomic analysis of type I polyketide synthase genes in pathogenic and saprobic ascomycetes
journal, December 2003

  • Kroken, S.; Glass, N. L.; Taylor, J. W.
  • Proceedings of the National Academy of Sciences, Vol. 100, Issue 26
  • DOI: 10.1073/pnas.2532165100

The Longibrachiatum Clade of Trichoderma: a revision with new species
journal, February 2012


Inferring duplications, losses, transfers and incomplete lineage sorting with nonbinary species trees.
text, January 2012

  • Stolzer, Maureen; Lai, Han; Xu, Minli
  • Carnegie Mellon University
  • DOI: 10.1184/r1/6099671

Improvement of Phylogenies after Removing Divergent and Ambiguously Aligned Blocks from Protein Sequence Alignments
journal, August 2007


Horizontal Transfer and Death of a Fungal Secondary Metabolic Gene Cluster
journal, January 2012

  • Campbell, Matthew A.; Rokas, Antonis; Slot, Jason C.
  • Genome Biology and Evolution, Vol. 4, Issue 3
  • DOI: 10.1093/gbe/evs011

New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0
text, January 2010

  • Guindon, Stéphane; Dufayard, Jean-François; Lefort, Vincent
  • Oxford University Press
  • DOI: 10.5167/uzh-155669

Genomic mutational analysis of the impact of the classical strain improvement program on β–lactam producing Penicillium chrysogenum
journal, November 2015


The Evolution of Fungal Metabolic Pathways
journal, December 2014


Fungal metabolic gene clusters—caravans traveling across genomes and environments
journal, March 2015


Horizontal gene transfer in osmotrophs: playing with public goods
journal, September 2013

  • Richards, Thomas A.; Talbot, Nicholas J.
  • Nature Reviews Microbiology, Vol. 11, Issue 10
  • DOI: 10.1038/nrmicro3108

Horizontal gene transfer, genome innovation and evolution
journal, August 2005

  • Gogarten, J. Peter; Townsend, Jeffrey P.
  • Nature Reviews Microbiology, Vol. 3, Issue 9
  • DOI: 10.1038/nrmicro1204

Horizontal Gene Transfer in Eukaryotic Plant Pathogens
journal, August 2014


Epigenetics as an emerging tool for improvement of fungal strains used in biotechnology
journal, June 2015

  • Aghcheh, Razieh Karimi; Kubicek, Christian P.
  • Applied Microbiology and Biotechnology, Vol. 99, Issue 15
  • DOI: 10.1007/s00253-015-6763-2

NADPH oxidases in fungi: Diverse roles of reactive oxygen species in fungal cellular differentiation
journal, November 2007


The Polyketide Synthase Gene pks4 of Trichoderma reesei Provides Pigmentation and Stress Resistance
journal, September 2013

  • Atanasova, Lea; Knox, Benjamin P.; Kubicek, Christian P.
  • Eukaryotic Cell, Vol. 12, Issue 11
  • DOI: 10.1128/EC.00103-13

Comparative analysis of the Trichoderma reesei transcriptome during growth on the cellulase inducing substrates wheat straw and lactose
journal, January 2013

  • Bischof, Robert; Fourtis, Lukas; Limbeck, Andreas
  • Biotechnology for Biofuels, Vol. 6, Issue 1
  • DOI: 10.1186/1754-6834-6-127

Acquisition of prokaryotic genes by fungal genomes
journal, January 2010


Draft Whole-Genome Sequence of Trichoderma gamsii T6085, a Promising Biocontrol Agent of Fusarium Head Blight on Wheat
journal, February 2016

  • Baroncelli, Riccardo; Zapparata, Antonio; Piaggeschi, Giulia
  • Genome Announcements, Vol. 4, Issue 1
  • DOI: 10.1128/genomeA.01747-15

Genomic mutational analysis of the impact of the classical strain improvement program on β–lactam producing Penicillium chrysogenum
journal, November 2015


T-REX: a web server for inferring, validating and visualizing phylogenetic trees and networks
journal, June 2012

  • Boc, A.; Diallo, A. B.; Makarenkov, V.
  • Nucleic Acids Research, Vol. 40, Issue W1
  • DOI: 10.1093/nar/gks485

A sand fly salivary protein acts as a neutrophil chemoattractant
journal, May 2021

  • Guimaraes-Costa, Anderson B.; Shannon, John P.; Waclawiak, Ingrid
  • Nature Communications, Vol. 12, Issue 1
  • DOI: 10.1038/s41467-021-23002-5

Horizontal transfer of an adaptive chimeric photoreceptor from bryophytes to ferns
journal, April 2014

  • Li, F. -W.; Villarreal, J. C.; Kelly, S.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 18
  • DOI: 10.1073/pnas.1319929111

Trichodimerol (BMS-182123) inhibits lipopolysaccharide-induced eicosanoid secretion in THP-1 human monocytic cells
journal, August 1996

  • Mazzucco, Charles E.; Warr, Glenn
  • Journal of Leukocyte Biology, Vol. 60, Issue 2
  • DOI: 10.1002/jlb.60.2.271

Inferring duplications, losses, transfers and incomplete lineage sorting with nonbinary species trees.
text, January 2012

  • Stolzer, Maureen; Lai, Han; Xu, Minli
  • Carnegie Mellon University
  • DOI: 10.1184/r1/6099671

The Longibrachiatum Clade of Trichoderma: a revision with new species
journal, February 2012


Chromatin-level regulation of biosynthetic gene clusters
journal, May 2009

  • Bok, Jin Woo; Chiang, Yi-Ming; Szewczyk, Edyta
  • Nature Chemical Biology, Vol. 5, Issue 7, p. 462-464
  • DOI: 10.1038/nchembio.177

Funybase: a Fungal phylogenomic database
journal, January 2008

  • Marthey, Sylvain; Aguileta, Gabriela; Rodolphe, Francois
  • BMC Bioinformatics, Vol. 9, Issue 1
  • DOI: 10.1186/1471-2105-9-456

MUSCLE: a multiple sequence alignment method with reduced time and space complexity
journal, August 2004


Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development
journal, August 2005


Inferring duplications, losses, transfers and incomplete lineage sorting with nonbinary species trees
journal, September 2012


Comparative genome sequence analysis underscores mycoparasitism as the ancestral life style of Trichoderma
journal, April 2011

  • Kubicek, Christian P.; Herrera-Estrella, Alfredo; Seidl-Seiboth, Verena
  • Genome Biology, Vol. 12, Issue 4
  • DOI: 10.1186/gb-2011-12-4-r40

Jane: a new tool for the cophylogeny reconstruction problem
journal, January 2010

  • Conow, Chris; Fielder, Daniel; Ovadia, Yaniv
  • Algorithms for Molecular Biology, Vol. 5, Issue 1
  • DOI: 10.1186/1748-7188-5-16

Horizontal Transfer of a Large and Highly Toxic Secondary Metabolic Gene Cluster between Fungi
journal, January 2011


GLOOME: gain loss mapping engine
journal, September 2010


Evidence for horizontal transfer of a secondary metabolite gene cluster between fungi
journal, January 2008

  • Khaldi, Nora; Collemare, Jérôme; Lebrun, Marc-Henri
  • Genome Biology, Vol. 9, Issue 1
  • DOI: 10.1186/gb-2008-9-1-r18

Eukaryote-to-eukaryote gene transfer events revealed by the genome sequence of the wine yeast Saccharomyces cerevisiae EC1118
journal, September 2009

  • Novo, M.; Bigey, F.; Beyne, E.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 38
  • DOI: 10.1073/pnas.0904673106

NOX enzymes and the biology of reactive oxygen
journal, March 2004

  • Lambeth, J. David
  • Nature Reviews Immunology, Vol. 4, Issue 3
  • DOI: 10.1038/nri1312

Explorations of fungal biosynthesis of reduced polyketides – a personal viewpoint
journal, January 2014


Investigating the beneficial traits of Trichoderma hamatum GD12 for sustainable agriculture—insights from genomics
journal, January 2013

  • Studholme, David J.; Harris, Beverley; Le Cocq, Kate
  • Frontiers in Plant Science, Vol. 4
  • DOI: 10.3389/fpls.2013.00258

Origin and distribution of epipolythiodioxopiperazine (ETP) gene clusters in filamentous ascomycetes
text, January 2007

  • Patron, Nicola J.; Waller, Ross F.; Cozijnsen, Anton J.
  • Springer Nature
  • DOI: 10.13016/pp8h-pkvd

Systems Analysis of Lactose Metabolism in Trichoderma reesei Identifies a Lactose Permease That Is Essential for Cellulase Induction
journal, May 2013


Evolutionary Origins of the Fumonisin Secondary Metabolite Gene Cluster in Fusarium verticillioides and Aspergillus niger
journal, January 2011

  • Khaldi, Nora; Wolfe, Kenneth H.
  • International Journal of Evolutionary Biology, Vol. 2011
  • DOI: 10.4061/2011/423821

Functional Analyses of Trichoderma reesei LAE1 Reveal Conserved and Contrasting Roles of This Regulator
journal, February 2013

  • Karimi-Aghcheh, Razieh; Bok, Jin Woo; Phatale, Pallavi A.
  • G3: Genes|Genomes|Genetics, Vol. 3, Issue 2
  • DOI: 10.1534/g3.112.005140

Multiple recent horizontal transfers of a large genomic region in cheese making fungi
journal, January 2014

  • Cheeseman, Kevin; Ropars, Jeanne; Renault, Pierre
  • Nature Communications, Vol. 5, Issue 1
  • DOI: 10.1038/ncomms3876

Sorbicillin Analogues and Related Dimeric Compounds from Penicillium n otatum
journal, June 2005

  • Maskey, Rajendra P.; Grün-Wollny, Iris; Laatsch, Hartmut
  • Journal of Natural Products, Vol. 68, Issue 6
  • DOI: 10.1021/np040137t

Molecular phylogeny and species delimitation in the section Longibrachiatum of Trichoderma
journal, May 2012

  • Druzhinina, Irina S.; Komoń-Zelazowska, Monika; Ismaiel, Adnan
  • Fungal Genetics and Biology, Vol. 49, Issue 5, p. 358-368
  • DOI: 10.1016/j.fgb.2012.02.004

Multiple GAL pathway gene clusters evolved independently and by different mechanisms in fungi
journal, May 2010

  • Slot, J. C.; Rokas, A.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 22
  • DOI: 10.1073/pnas.0914418107

Horizontal Transfer and Death of a Fungal Secondary Metabolic Gene Cluster
journal, January 2012

  • Campbell, Matthew A.; Rokas, Antonis; Slot, Jason C.
  • Genome Biology and Evolution, Vol. 4, Issue 3
  • DOI: 10.1093/gbe/evs011

Genome-scale phylogenetic analysis finds extensive gene transfer among fungi
journal, September 2015

  • Szöllősi, Gergely J.; Davín, Adrián Arellano; Tannier, Eric
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 370, Issue 1678
  • DOI: 10.1098/rstb.2014.0335

Novel Oxidized Sorbicillin Dimers with 1,1-Diphenyl-2-picrylhydrazyl-Radical Scavenging Activity from a Fungus
journal, January 1998

  • Abe, Naoki; Murata, Takashi; Hirota, Akira
  • Bioscience, Biotechnology, and Biochemistry, Vol. 62, Issue 11
  • DOI: 10.1271/bbb.62.2120

Networks of Gene Sharing among 329 Proteobacterial Genomes Reveal Differences in Lateral Gene Transfer Frequency at Different Phylogenetic Depths
journal, November 2010

  • Kloesges, T.; Popa, O.; Martin, W.
  • Molecular Biology and Evolution, Vol. 28, Issue 2
  • DOI: 10.1093/molbev/msq297

Evidence for horizontal transfer of a secondary metabolite gene cluster between fungi
journal, January 2008

  • Khaldi, Nora; Collemare, Jérôme; Lebrun, Marc-Henri
  • Genome Biology, Vol. 9, Issue 1
  • DOI: 10.1186/gb-2008-9-1-r18

The sorbicillinoid family of natural products: Isolation, biosynthesis, and synthetic studies
journal, January 2011

  • Harned, Andrew M.; Volp, Kelly A.
  • Natural Product Reports, Vol. 28, Issue 11
  • DOI: 10.1039/c1np00039j

Origin and distribution of epipolythiodioxopiperazine (ETP) gene clusters in filamentous ascomycetes
journal, January 2007

  • Patron, Nicola J.; Waller, Ross F.; Cozijnsen, Anton J.
  • BMC Evolutionary Biology, Vol. 7, Issue 1
  • DOI: 10.1186/1471-2148-7-174

Phylogenomic analysis of polyketide synthase-encoding genes in Trichoderma
journal, November 2011


A complete annotation of the chromosomes of the cellulase producer Trichoderma reesei provides insights in gene clusters, their expression and reveals genes required for fitness
journal, March 2016

  • Druzhinina, Irina S.; Kopchinskiy, Alexey G.; Kubicek, Eva M.
  • Biotechnology for Biofuels, Vol. 9, Issue 1
  • DOI: 10.1186/s13068-016-0488-z

A comparison of normalization methods for high density oligonucleotide array data based on variance and bias
journal, January 2003


Ancient Horizontal Gene Transfer from Bacteria Enhances Biosynthetic Capabilities of Fungi
journal, February 2009


Fungal polyketide biosynthesis – a personal perspective
journal, January 2014


Summaries of Affymetrix GeneChip probe level data
journal, February 2003


Concerted and Birth-and-Death Evolution of Multigene Families
journal, December 2005


Horizontal gene transfer, genome innovation and evolution
journal, August 2005

  • Gogarten, J. Peter; Townsend, Jeffrey P.
  • Nature Reviews Microbiology, Vol. 3, Issue 9
  • DOI: 10.1038/nrmicro1204

The metabolites of Trichoderma longibrachiatum. Part II The structures of trichodermolide and sorbiquinol
journal, March 1996

  • Andrade, Romano; Ayer, William A.; Trifonov, Latchezar S.
  • Canadian Journal of Chemistry, Vol. 74, Issue 3
  • DOI: 10.1139/v96-042

Epigenetics as an emerging tool for improvement of fungal strains used in biotechnology
journal, June 2015

  • Aghcheh, Razieh Karimi; Kubicek, Christian P.
  • Applied Microbiology and Biotechnology, Vol. 99, Issue 15
  • DOI: 10.1007/s00253-015-6763-2

The metabolites of Trichoderma longibrachiatum. Part II The structures of trichodermolide and sorbiquinol
journal, March 1996

  • Andrade, Romano; Ayer, William A.; Trifonov, Latchezar S.
  • Canadian Journal of Chemistry, Vol. 74, Issue 3
  • DOI: 10.1139/v96-042

Inferring and Validating Horizontal Gene Transfer Events Using Bipartition Dissimilarity
journal, January 2010

  • Boc, Alix; Philippe, Hervé; Makarenkov, Vladimir
  • Systematic Biology, Vol. 59, Issue 2
  • DOI: 10.1093/sysbio/syp103

Comparative transcriptomics reveals different strategies of Trichoderma mycoparasitism
journal, January 2013


Trichodimerol (BMS-182123) inhibits lipopolysaccharide-induced eicosanoid secretion in THP-1 human monocytic cells
journal, August 1996

  • Mazzucco, Charles E.; Warr, Glenn
  • Journal of Leukocyte Biology, Vol. 60, Issue 2
  • DOI: 10.1002/jlb.60.2.271

Eukaryote-to-eukaryote gene transfer events revealed by the genome sequence of the wine yeast Saccharomyces cerevisiae EC1118
journal, September 2009

  • Novo, M.; Bigey, F.; Beyne, E.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 38
  • DOI: 10.1073/pnas.0904673106

Identification of the Main Regulator Responsible for Synthesis of the Typical Yellow Pigment Produced by Trichoderma reesei
journal, August 2016

  • Derntl, Christian; Rassinger, Alice; Srebotnik, Ewald
  • Applied and Environmental Microbiology, Vol. 82, Issue 20
  • DOI: 10.1128/AEM.01408-16

A complete annotation of the chromosomes of the cellulase producer Trichoderma reesei provides insights in gene clusters, their expression and reveals genes required for fitness
journal, March 2016

  • Druzhinina, Irina S.; Kopchinskiy, Alexey G.; Kubicek, Eva M.
  • Biotechnology for Biofuels, Vol. 9, Issue 1
  • DOI: 10.1186/s13068-016-0488-z

Oxidative dearomatisation: the key step of sorbicillinoid biosynthesis
other, January 2013

  • Al-Fahad, Ahmed; Abood, Amira; Fisch, Katja M.
  • Cambridge : Royal Society of Chemistry
  • DOI: 10.15488/124

GLOOME: gain loss mapping engine
journal, September 2010


T-REX: a web server for inferring, validating and visualizing phylogenetic trees and networks
journal, June 2012

  • Boc, A.; Diallo, A. B.; Makarenkov, V.
  • Nucleic Acids Research, Vol. 40, Issue W1
  • DOI: 10.1093/nar/gks485

DnaSP v5: a software for comprehensive analysis of DNA polymorphism data
journal, April 2009


Identification of a Polyketide Synthase Involved in Sorbicillin Biosynthesis by Penicillium chrysogenum
journal, April 2016

  • Salo, Oleksandr; Guzmán-Chávez, Fernando; Ries, Marco I.
  • Applied and Environmental Microbiology, Vol. 82, Issue 13
  • DOI: 10.1128/AEM.00350-16

Inferring duplications, losses, transfers and incomplete lineage sorting with nonbinary species trees.
text, January 2012


Modular networks and cumulative impact of lateral transfer in prokaryote genome evolution
journal, July 2008

  • Dagan, T.; Artzy-Randrup, Y.; Martin, W.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue 29
  • DOI: 10.1073/pnas.0800679105

Genome-scale phylogenetic analysis finds extensive gene transfer among Fungi
preprint, January 2015


Genomic insights into the distribution, genetic diversity and evolution of polyketide synthases and nonribosomal peptide synthetases
journal, December 2015

  • Wang, Hao; Sivonen, Kaarina; Fewer, David P.
  • Current Opinion in Genetics & Development, Vol. 35
  • DOI: 10.1016/j.gde.2015.10.004

Phylogenomic Analysis Demonstrates a Pattern of Rare and Ancient Horizontal Gene Transfer between Plants and Fungi
journal, July 2009

  • Richards, Thomas A.; Soanes, Darren M.; Foster, Peter G.
  • The Plant Cell, Vol. 21, Issue 7
  • DOI: 10.1105/tpc.109.065805

Bisvertinols: a new group of dimeric vertinoids from
journal, January 1986


Jane: a new tool for the cophylogeny reconstruction problem
journal, January 2010

  • Conow, Chris; Fielder, Daniel; Ovadia, Yaniv
  • Algorithms for Molecular Biology, Vol. 5, Issue 1
  • DOI: 10.1186/1748-7188-5-16

Oxidative dearomatisation: the key step of sorbicillinoid biosynthesis
journal, January 2014

  • Fahad, Ahmed al; Abood, Amira; Fisch, Katja M.
  • Chem. Sci., Vol. 5, Issue 2
  • DOI: 10.1039/C3SC52911H

Fungal metabolic gene clusters—caravans traveling across genomes and environments
journal, March 2015


New Algorithms and Methods to Estimate Maximum-Likelihood Phylogenies: Assessing the Performance of PhyML 3.0
text, January 2010


Inferring parsimonious migration histories for metastatic cancers
journal, April 2018


Expression of Biomass-Degrading Enzymes Is a Major Event during Conidium Development in Trichoderma reesei
journal, September 2011

  • Metz, Benjamin; Seidl-Seiboth, Verena; Haarmann, Thomas
  • Eukaryotic Cell, Vol. 10, Issue 11
  • DOI: 10.1128/ec.05014-11

The Evolution of Fungal Metabolic Pathways
journal, December 2014


A fungal phylogeny based on 82 complete genomes using the composition vector method
journal, January 2009


Genes Acquired by Horizontal Transfer Are Potentially Involved in the Evolution of Phytopathogenicity in Moniliophthora perniciosa and Moniliophthora roreri, Two of the Major Pathogens of Cacao
journal, December 2009

  • Tiburcio, Ricardo Augusto; Costa, Gustavo Gilson Lacerda; Carazzolle, Marcelo Falsarella
  • Journal of Molecular Evolution, Vol. 70, Issue 1
  • DOI: 10.1007/s00239-009-9311-9

Peroxide accumulation and cell death in filamentous fungi induced by contact with a contestant
journal, February 2005


Funybase: a Fungal phylogenomic database
journal, January 2008

  • Marthey, Sylvain; Aguileta, Gabriela; Rodolphe, Francois
  • BMC Bioinformatics, Vol. 9, Issue 1
  • DOI: 10.1186/1471-2105-9-456

Comparative Genomics Provide Insights into Evolution of Trichoderma Nutrition Style
journal, January 2014

  • Xie, Bin-Bin; Qin, Qi-Long; Shi, Mei
  • Genome Biology and Evolution, Vol. 6, Issue 2
  • DOI: 10.1093/gbe/evu018

Lower Citrinin Production by Gene Disruption of ctnB Involved in Citrinin Biosynthesis in Monascus aurantiacus Li AS3.4384
journal, July 2013

  • Li, Yan-Ping; Pan, Yi-Feng; Zou, Le-Hua
  • Journal of Agricultural and Food Chemistry, Vol. 61, Issue 30
  • DOI: 10.1021/jf400879s

Comparative analysis of the Trichoderma reesei transcriptome during growth on the cellulase inducing substrates wheat straw and lactose
journal, January 2013

  • Bischof, Robert; Fourtis, Lukas; Limbeck, Andreas
  • Biotechnology for Biofuels, Vol. 6, Issue 1
  • DOI: 10.1186/1754-6834-6-127

Horizontal Gene Transfer in Eukaryotic Plant Pathogens
journal, August 2014


Works referencing / citing this record:

Evolutionary and functional patterns of shared gene neighbourhood in fungi
journal, September 2019


The diversity of Trichoderma species from soil in South Africa, with five new additions
journal, May 2018


Gene regulation associated with sexual development and female fertility in different isolates of Trichoderma reesei
journal, May 2018

  • Dattenböck, Christoph; Tisch, Doris; Schuster, Andre
  • Fungal Biology and Biotechnology, Vol. 5, Issue 1
  • DOI: 10.1186/s40694-018-0055-4

Constitutive hyperproduction of sorbicillinoids in Trichoderma reesei ZC121
journal, October 2018


Engineering of the Filamentous Fungus Penicillium chrysogenum as Cell Factory for Natural Products
journal, November 2018

  • Guzmán-Chávez, Fernando; Zwahlen, Reto D.; Bovenberg, Roel A. L.
  • Frontiers in Microbiology, Vol. 9
  • DOI: 10.3389/fmicb.2018.02768

Analysis of the hybrid genomes of two field isolates of the soil-borne fungal species Verticillium longisporum
journal, January 2018


Analysis of the hybrid genomes of two field isolates of the soil-borne fungal species Verticillium longisporum
journal, January 2018