Functional Analyses of Trichoderma reesei LAE1 Reveal Conserved and Contrasting Roles of This Regulator
Abstract
The putative methyltransferase LaeA is a global regulator that affects the expression of multiple secondary metabolite gene clusters in several fungi, and it can modify heterochromatin structure in Aspergillus nidulans. We have recently shown that the LaeA ortholog of Trichoderma reesei (LAE1), a fungus that is an industrial producer of cellulase and hemicellulase enzymes, regulates the expression of cellulases and polysaccharide hydrolases. To learn more about the function of LAE1 in T. reesei, we analyzied the effect of deletion and overexpression of lae1 on genome-wide gene expression. We discovered that in addition to positively regulating 7 of 17 polyketide or nonribosomal peptide synthases, genes encoding ankyrin-proteins, iron uptake, heterokaryon incompatibility proteins, PTH11-receptors, and oxidases/monoxygenases are major gene categories also regulated by LAE1. chromatin immunoprecipitation sequencing with antibodies against histone modifications known to be associated with transcriptionally active (H3K4me2 and -me3) or silent (H3K9me3) chromatin detected 4089 genes bearing one or more of these methylation marks, of which 75 exhibited a correlation between either H3K4me2 or H3K4me3 and regulation by LAE1. Transformation of a laeA-null mutant of A. nidulans with the T. reesei lae1 gene did not rescue sterigmatocystin formation and further impaired sexual development. LAE1 did not interact with A.more » VeA in yeast two-hybrid assays, whereas it interacted with the T. reesei VeA ortholog, VEL1. LAE1 was shown to be required for the expression of vel1, whereas the orthologs of velB and VosA are unaffected by lae1 deletion. Our data show that the biological roles of A. nidulans LaeA and T. reesei LAE1 are much less conserved than hitherto thought. In T. reesei, LAE1 appears predominantly to regulate genes increasing relative fitness in its environment.
- Authors:
-
[4];
- Vienna Univ. of Technology (Austria)
- Univ. of Wisconsin-Madison, Madison, WI (United States)
- Oregon State Univ., Corvallis, OR (United States)
- Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
- Publication Date:
- Research Org.:
- Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
- Sponsoring Org.:
- USDOE; National Institutes of Health (NIH)
- OSTI Identifier:
- 1557228
- Report Number(s):
- PNNL-SA-94192
Journal ID: ISSN 2160-1836
- Grant/Contract Number:
- AC05-76RL01830
- Resource Type:
- Accepted Manuscript
- Journal Name:
- G3
- Additional Journal Information:
- Journal Volume: 3; Journal Issue: 2; Journal ID: ISSN 2160-1836
- Publisher:
- Genetics Society of America
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Trichoderma; epigenetic
Citation Formats
Karimi-Aghcheh, Razieh, Bok, Jin Woo, Phatale, Pallavi A., Smith, Kristina M., Baker, Scott E., Lichius, Alexander, Omann, Markus, Zeilinger, Susanne, Seiboth, Bernhard, Rhee, Catherine, Keller, Nancy P., Freitag, Michael, and Kubicek, Christian P. Functional Analyses of Trichoderma reesei LAE1 Reveal Conserved and Contrasting Roles of This Regulator. United States: N. p., 2013.
Web. doi:10.1534/g3.112.005140.
Karimi-Aghcheh, Razieh, Bok, Jin Woo, Phatale, Pallavi A., Smith, Kristina M., Baker, Scott E., Lichius, Alexander, Omann, Markus, Zeilinger, Susanne, Seiboth, Bernhard, Rhee, Catherine, Keller, Nancy P., Freitag, Michael, & Kubicek, Christian P. Functional Analyses of Trichoderma reesei LAE1 Reveal Conserved and Contrasting Roles of This Regulator. United States. doi:10.1534/g3.112.005140.
Karimi-Aghcheh, Razieh, Bok, Jin Woo, Phatale, Pallavi A., Smith, Kristina M., Baker, Scott E., Lichius, Alexander, Omann, Markus, Zeilinger, Susanne, Seiboth, Bernhard, Rhee, Catherine, Keller, Nancy P., Freitag, Michael, and Kubicek, Christian P. Fri .
"Functional Analyses of Trichoderma reesei LAE1 Reveal Conserved and Contrasting Roles of This Regulator". United States. doi:10.1534/g3.112.005140. https://www.osti.gov/servlets/purl/1557228.
@article{osti_1557228,
title = {Functional Analyses of Trichoderma reesei LAE1 Reveal Conserved and Contrasting Roles of This Regulator},
author = {Karimi-Aghcheh, Razieh and Bok, Jin Woo and Phatale, Pallavi A. and Smith, Kristina M. and Baker, Scott E. and Lichius, Alexander and Omann, Markus and Zeilinger, Susanne and Seiboth, Bernhard and Rhee, Catherine and Keller, Nancy P. and Freitag, Michael and Kubicek, Christian P.},
abstractNote = {The putative methyltransferase LaeA is a global regulator that affects the expression of multiple secondary metabolite gene clusters in several fungi, and it can modify heterochromatin structure in Aspergillus nidulans. We have recently shown that the LaeA ortholog of Trichoderma reesei (LAE1), a fungus that is an industrial producer of cellulase and hemicellulase enzymes, regulates the expression of cellulases and polysaccharide hydrolases. To learn more about the function of LAE1 in T. reesei, we analyzied the effect of deletion and overexpression of lae1 on genome-wide gene expression. We discovered that in addition to positively regulating 7 of 17 polyketide or nonribosomal peptide synthases, genes encoding ankyrin-proteins, iron uptake, heterokaryon incompatibility proteins, PTH11-receptors, and oxidases/monoxygenases are major gene categories also regulated by LAE1. chromatin immunoprecipitation sequencing with antibodies against histone modifications known to be associated with transcriptionally active (H3K4me2 and -me3) or silent (H3K9me3) chromatin detected 4089 genes bearing one or more of these methylation marks, of which 75 exhibited a correlation between either H3K4me2 or H3K4me3 and regulation by LAE1. Transformation of a laeA-null mutant of A. nidulans with the T. reesei lae1 gene did not rescue sterigmatocystin formation and further impaired sexual development. LAE1 did not interact with A. nidulans VeA in yeast two-hybrid assays, whereas it interacted with the T. reesei VeA ortholog, VEL1. LAE1 was shown to be required for the expression of vel1, whereas the orthologs of velB and VosA are unaffected by lae1 deletion. Our data show that the biological roles of A. nidulans LaeA and T. reesei LAE1 are much less conserved than hitherto thought. In T. reesei, LAE1 appears predominantly to regulate genes increasing relative fitness in its environment.},
doi = {10.1534/g3.112.005140},
journal = {G3},
number = 2,
volume = 3,
place = {United States},
year = {2013},
month = {2}
}
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The global regulator LaeA controls penicillin biosynthesis, pigmentation and sporulation, but not roquefortine C synthesis in Penicillium chrysogenum
journal, February 2009
- Kosalková, Katarina; García-Estrada, Carlos; Ullán, Ricardo V.
- Biochimie, Vol. 91, Issue 2
Genomic Mining for Aspergillus Natural Products
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- Bok, Jin Woo; Hoffmeister, Dirk; Maggio-Hall, Lori A.
- Chemistry & Biology, Vol. 13, Issue 1
Histone arginine methylation
journal, November 2010
- Di Lorenzo, Alessandra; Bedford, Mark T.
- FEBS Letters, Vol. 585, Issue 13
Accurate prediction of the Aspergillus nidulans terrequinone gene cluster boundaries using the transcriptional regulator LaeA
journal, November 2007
- Bouhired, Sarah; Weber, Monika; Kempf-Sontag, Anita
- Fungal Genetics and Biology, Vol. 44, Issue 11, p. 1134-1145
Neurospora crassa ve-1 affects asexual conidiation
journal, February 2008
- Bayram, Özgür; Krappmann, Sven; Seiler, Stephan
- Fungal Genetics and Biology, Vol. 45, Issue 2
Requirement of LaeA for secondary metabolism and sclerotial production in Aspergillus flavus
journal, October 2008
- Kale, Shubha P.; Milde, Lane; Trapp, Marisa K.
- Fungal Genetics and Biology, Vol. 45, Issue 10, p. 1422-1429
Regulation of secondary metabolism by chromatin structure and epigenetic codes
journal, January 2011
- Strauss, Joseph; Reyes-Dominguez, Yazmid
- Fungal Genetics and Biology, Vol. 48, Issue 1
Lae1 regulates expression of multiple secondary metabolite gene clusters in Fusarium verticillioides
journal, August 2012
- Butchko, Robert A. E.; Brown, Daren W.; Busman, Mark
- Fungal Genetics and Biology, Vol. 49, Issue 8, p. 602-612
FgVELB is associated with vegetative differentiation, secondary metabolism and virulence in Fusarium graminearum
journal, August 2012
- Jiang, Jinhua; Yun, Yingzi; Liu, Ye
- Fungal Genetics and Biology, Vol. 49, Issue 8
Effects of laeA deletion on Aspergillus flavus conidial development and hydrophobicity may contribute to loss of aflatoxin production
journal, February 2012
- Chang, Perng-Kuang; Scharfenstein, Leslie L.; Ehrlich, Kenneth C.
- Fungal Biology, Vol. 116, Issue 2
RF cloning: A restriction-free method for inserting target genes into plasmids
journal, April 2006
- van den Ent, Fusinita; Löwe, Jan
- Journal of Biochemical and Biophysical Methods, Vol. 67, Issue 1
Genome-wide high throughput analysis of DNA methylation in eukaryotes
journal, March 2009
- Pomraning, Kyle R.; Smith, Kristina M.; Freitag, Michael
- Methods, Vol. 47, Issue 3
Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease
journal, November 1979
- Chirgwin, John M.; Przybyla, Alan E.; MacDonald, Raymond J.
- Biochemistry, Vol. 18, Issue 24
A histone H3 methyltransferase controls DNA methylation in Neurospora crassa
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- Tamaru, Hisashi; Selker, Eric U.
- Nature, Vol. 414, Issue 6861
Genome sequencing and analysis of the biomass-degrading fungus Trichoderma reesei (syn. Hypocrea jecorina)
journal, May 2008
- Martinez, Diego; Berka, Randy M.; Henrissat, Bernard
- Nature Biotechnology, Vol. 26, Issue 5
Trimethylated lysine 9 of histone H3 is a mark for DNA methylation in Neurospora crassa
journal, April 2003
- Tamaru, Hisashi; Zhang, Xing; McMillen, Debra
- Nature Genetics, Vol. 34, Issue 1
Trichoderma: the genomics of opportunistic success
journal, September 2011
- Druzhinina, Irina S.; Seidl-Seiboth, Verena; Herrera-Estrella, Alfredo
- Nature Reviews Microbiology, Vol. 9, Issue 10
Structure of the Conserved Core of the Yeast Dot1p, a Nucleosomal Histone H3 Lysine 79 Methyltransferase
journal, July 2004
- Sawada, Ken; Yang, Zhe; Horton, John R.
- Journal of Biological Chemistry, Vol. 279, Issue 41
A comparison of normalization methods for high density oligonucleotide array data based on variance and bias
journal, January 2003
- Bolstad, B. M.; Irizarry, R. A.; Astrand, M.
- Bioinformatics, Vol. 19, Issue 2
Relative expression software tool (REST(C)) for group-wise comparison and statistical analysis of relative expression results in real-time PCR
journal, May 2002
- Pfaffl, M. W.
- Nucleic Acids Research, Vol. 30, Issue 9
The FunCat, a functional annotation scheme for systematic classification of proteins from whole genomes
journal, October 2004
- Ruepp, A.
- Nucleic Acids Research, Vol. 32, Issue 18
Summaries of Affymetrix GeneChip probe level data
journal, February 2003
- Irizarry, R. A.
- Nucleic Acids Research, Vol. 31, Issue 4
Phylogenomic analysis of polyketide synthase-encoding genes in Trichoderma
journal, November 2011
- Baker, S. E.; Perrone, G.; Richardson, N. M.
- Microbiology, Vol. 158, Issue 1
Intact-cell MALDI-TOF mass spectrometry analysis of peptaibol formation by the genus Trichoderma/Hypocrea: can molecular phylogeny of species predict peptaibol structures?
journal, October 2007
- Neuhof, T.; Dieckmann, R.; Druzhinina, I. S.
- Microbiology, Vol. 153, Issue 10
Relics of repeat-induced point mutation direct heterochromatin formation in Neurospora crassa
journal, December 2008
- Lewis, Z. A.; Honda, S.; Khlafallah, T. K.
- Genome Research, Vol. 19, Issue 3
Beyond aflatoxin: four distinct expression patterns and functional roles associated with Aspergillus flavus secondary metabolism gene clusters
journal, March 2010
- Georgianna, D. Ryan; Fedorova, Natalie D.; Burroughs, James L.
- Molecular Plant Pathology, Vol. 11, Issue 2, p. 213-226
Secondary metabolic gene cluster silencing in Aspergillus nidulans
journal, September 2006
- Bok, Jin Woo; Noordermeer, Daan; Kale, Shubha P.
- Molecular Microbiology, Vol. 61, Issue 6, p. 1636-1645
Heterochromatic marks are associated with the repression of secondary metabolism clusters in Aspergillus nidulans
journal, February 2010
- Reyes-Dominguez, Yazmid; Bok, Jin Woo; Berger, Harald
- Molecular Microbiology, Vol. 76, Issue 6, p. 1376-1386
FfVel1 and FfLae1, components of a velvet-like complex in Fusarium fujikuroi, affect differentiation, secondary metabolism and virulence: Identification of a velvet-like complex in F. fujikuroi
journal, July 2010
- Wiemann, Philipp; Brown, Daren W.; Kleigrewe, Karin
- Molecular Microbiology
The putative protein methyltransferase LAE1 controls cellulase gene expression in Trichoderma reesei: Cellulase regulation in T. reesei
journal, May 2012
- Seiboth, Bernhard; Karimi, Razieh Aghcheh; Phatale, Pallavi A.
- Molecular Microbiology, Vol. 84, Issue 6
Overexpression of the Aspergillus nidulans histone 4 acetyltransferase EsaA increases activation of secondary metabolite production
journal, August 2012
- Soukup, Alexandra A.; Chiang, Yi-Ming; Bok, Jin Woo
- Molecular Microbiology, Vol. 86, Issue 2, p. 314-330
Novel traits of Trichoderma predicted through the analysis of its secretome
journal, September 2012
- Druzhinina, Irina S.; Shelest, Ekaterina; Kubicek, Christian P.
- FEMS Microbiology Letters, Vol. 337, Issue 1
Coordination of secondarymetabolism and development in fungi: the velvet familyof regulatory proteins
journal, January 2012
- Bayram, Özgür; Braus, Gerhard H.
- FEMS Microbiology Reviews, Vol. 36, Issue 1
VelB/VeA/LaeA Complex Coordinates Light Signal with Fungal Development and Secondary Metabolism
journal, June 2008
- Bayram, O.; Krappmann, S.; Ni, M.
- Science, Vol. 320, Issue 5882, p. 1504-1506
Roles of Protein Kinase A and Adenylate Cyclase in Light-Modulated Cellulase Regulation in Trichoderma reesei
journal, January 2012
- Schuster, André; Tisch, Doris; Seidl-Seiboth, Verena
- Applied and Environmental Microbiology, Vol. 78, Issue 7
Two Components of a velvet -Like Complex Control Hyphal Morphogenesis, Conidiophore Development, and Penicillin Biosynthesis in Penicillium chrysogenum
journal, June 2010
- Hoff, Birgit; Kamerewerd, Jens; Sigl, Claudia
- Eukaryotic Cell, Vol. 9, Issue 8
Distinct Roles for VeA and LaeA in Development and Pathogenesis of Aspergillus flavus
journal, May 2009
- Amaike, Saori; Keller, Nancy P.
- Eukaryotic Cell, Vol. 8, Issue 7
Role of laeA in the Regulation of alb1 , gliP , Conidial Morphology, and Virulence in Aspergillus fumigatus
journal, July 2007
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