Functional Analyses of Trichoderma reesei LAE1 Reveal Conserved and Contrasting Roles of This Regulator

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.

doi:10.1534/g3.112.005140

Functional Analyses of Trichoderma reesei LAE1 Reveal Conserved and Contrasting Roles of This Regulator

Journal Article · Fri Feb 01 00:00:00 EST 2013 · G3

DOI:https://doi.org/10.1534/g3.112.005140· OSTI ID:1557228

Karimi-Aghcheh, Razieh ^[1]; Bok, Jin Woo ^[2]; Phatale, Pallavi A. ^[3]; Smith, Kristina M. ^[3]; ^[4]; Lichius, Alexander ^[1]; Omann, Markus ^[1]; Zeilinger, Susanne ^[1]; Seiboth, Bernhard ^[1]; Rhee, Catherine ^[2]; Keller, Nancy P. ^[2]; Freitag, Michael ^[4]; Kubicek, Christian P. ^[1]

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)

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.

View Accepted Manuscript (DOE)

Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

Sponsoring Organization:: National Institutes of Health (NIH); USDOE

Grant/Contract Number:: AC05-76RL01830

OSTI ID:: 1557228

Report Number(s):: PNNL-SA--94192

Journal Information:: G3, Journal Name: G3 Journal Issue: 2 Vol. 3; ISSN 2160-1836

Publisher:: Genetics Society of AmericaCopyright Statement

Country of Publication:: United States

Language:: English

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A Novel Automethylation Reaction in the Aspergillus nidulans LaeA Protein Generates S -Methylmethionine Patananan, Alexander N.; Palmer, Jonathan M.; Garvey, Graeme S. Journal of Biological Chemistry, Vol. 288, Issue 20 https://doi.org/10.1074/jbc.m113.465765	journal	March 2013
A LaeA- and BrlA-dependent cellular network governs tissue-specific secondary metabolism in the human pathogen Aspergillus fumigatus Lind, Abigail L.; Lim, Fang Yun; Soukup, Alexandra A. mSphere https://doi.org/10.1101/196600	posted_content	September 2017
The Polyketide Synthase Gene pks4 of Trichoderma reesei Provides Pigmentation and Stress Resistance Atanasova, Lea; Knox, Benjamin P.; Kubicek, Christian P. Eukaryotic Cell, Vol. 12, Issue 11 https://doi.org/10.1128/ec.00103-13	journal	September 2013
Rapid Phenotypic and Metabolomic Domestication of Wild Penicillium Molds on Cheese Bodinaku, Ina; Shaffer, Jason; Connors, Allison B. mBio, Vol. 10, Issue 5 https://doi.org/10.1128/mbio.02445-19	journal	October 2019
The Genomes of Three Uneven Siblings: Footprints of the Lifestyles of Three Trichoderma Species Schmoll, Monika; Dattenböck, Christoph; Carreras-Villaseñor, Nohemí Microbiology and Molecular Biology Reviews, Vol. 80, Issue 1 https://doi.org/10.1128/mmbr.00040-15	journal	February 2016
Several steps of lateral gene transfer followed by events of ‘birth-and-death’ evolution shaped a fungal sorbicillinoid biosynthetic gene cluster Druzhinina, Irina S.; Kubicek, Eva M.; Kubicek, Christian P. BMC Evolutionary Biology, Vol. 16, Issue 1 https://doi.org/10.1186/s12862-016-0834-6	journal	December 2016
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 Druzhinina, Irina S.; Kopchinskiy, Alexey G.; Kubicek, Eva M. Biotechnology for Biofuels, Vol. 9, Issue 1 https://doi.org/10.1186/s13068-016-0488-z	journal	March 2016
Regulators of plant biomass degradation in ascomycetous fungi Benocci, Tiziano; Aguilar-Pontes, Maria Victoria; Zhou, Miaomiao Biotechnology for Biofuels, Vol. 10, Issue 1 https://doi.org/10.1186/s13068-017-0841-x	journal	June 2017
Moulding the mould: understanding and reprogramming filamentous fungal growth and morphogenesis for next generation cell factories Cairns, Timothy C.; Zheng, Xiaomei; Zheng, Ping Biotechnology for Biofuels, Vol. 12, Issue 1 https://doi.org/10.1186/s13068-019-1400-4	journal	April 2019
Gene regulation associated with sexual development and female fertility in different isolates of Trichoderma reesei Dattenböck, Christoph; Tisch, Doris; Schuster, Andre Fungal Biology and Biotechnology, Vol. 5, Issue 1 https://doi.org/10.1186/s40694-018-0055-4	journal	May 2018
The Putative Protein Methyltransferase LAE1 of Trichoderma atroviride Is a Key Regulator of Asexual Development and Mycoparasitism Aghcheh, Razieh Karimi; Druzhinina, Irina S.; Kubicek, Christian P. PLoS ONE, Vol. 8, Issue 6 https://doi.org/10.1371/journal.pone.0067144	journal	June 2013
The Different Roles of Penicillium oxalicum LaeA in the Production of Extracellular Cellulase and β-xylosidase Li, Yanan; Zheng, Xiaoju; Zhang, Xiujun Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.02091	journal	December 2016

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