The Polyketide Synthase Gene pks4 of Trichoderma reesei Provides Pigmentation and Stress Resistance

Atanasova, Lea; Knox, Benjamin P.; Kubicek, Christian P.; Druzhinina, Irina; Baker, Scott E.

doi:10.1128/EC.00103-13

The Polyketide Synthase Gene pks4 of Trichoderma reesei Provides Pigmentation and Stress Resistance

Journal Article · Fri Nov 01 00:00:00 EDT 2013 · Eukaryotic Cell

DOI:https://doi.org/10.1128/EC.00103-13· OSTI ID:1776806

Atanasova, Lea ^[1]; Knox, Benjamin P. ^[2]; Kubicek, Christian P. ^[3]; Druzhinina, Irina ^[3]; ^[2]

Vienna University of Technology
BATTELLE (PACIFIC NW LAB)
Technische Universitat Wien

Species of the fungal genus Trichoderma (Hypocreales, Ascomycota) are well-known for their production of various secondary metabolites. Nonribosomal peptides and polyketides represent a major portion of these products. In a recent phylogenomic investigation of Trichoderma polyketide synthase (PKS)-encoding genes, the pks4 from T. reesei was shown to be an orthologue of pigment-forming PKSs involved in synthesis of aurofusarin and bikaverin in Fusarium spp. In this study, we show that deletion of this gene in T. reesei results in loss of green conidial pigmentation and in pigmentation alteration of teleomorph structures. It also has an impact on conidial cell wall stability and the antagonistic abilities of T. reesei against other fungi, including formation of inhibitory metabolites. In addition, deletion of pks4 significantly influences the expression of other PKS-encoding genes of T. reesei. To our knowledge, this is the first indication that a low-molecular-weight pigment-forming PKS is involved in defense, mechanical stability, and stress resistance in fungi.

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

Sponsoring Organization:: USDOE

DOE Contract Number:: AC05-76RL01830

OSTI ID:: 1776806

Report Number(s):: PNNL-SA-100641

Journal Information:: Eukaryotic Cell, Journal Name: Eukaryotic Cell Journal Issue: 11 Vol. 12

Country of Publication:: United States

Language:: English

References (61)

Expression of Biomass-Degrading Enzymes Is a Major Event during Conidium Development in Trichoderma reesei Metz, Benjamin; Seidl-Seiboth, Verena; Haarmann, Thomas Eukaryotic Cell, Vol. 10, Issue 11 https://doi.org/10.1128/EC.05014-11	journal	September 2011
Separation and Identification of Volatile Compounds from Liquid Cultures of Trichoderma harzianum by GC-MS using Three Different Capillary Columns Siddiquee, S.; Cheong, B. E.; Taslima, K. Journal of Chromatographic Science, Vol. 50, Issue 4 https://doi.org/10.1093/chromsci/bms012	journal	March 2012
Phylogenomic analysis of type I polyketide synthase genes in pathogenic and saprobic ascomycetes Kroken, S.; Glass, N. L.; Taylor, J. W. Proceedings of the National Academy of Sciences, Vol. 100, Issue 26 https://doi.org/10.1073/pnas.2532165100	journal	December 2003
Enhancing the Stress Tolerance and Virulence of an Entomopathogen by Metabolic Engineering of Dihydroxynaphthalene Melanin Biosynthesis Genes Tseng, Min N.; Chung, Pei C.; Tzean, Shean S. Applied and Environmental Microbiology, Vol. 77, Issue 13 https://doi.org/10.1128/AEM.02033-10	journal	May 2011
Melanin and virulence in Cryptococcus neoformans Casadevall, Arturo; Rosas, Angel L.; Nosanchuk, Joshua D. Current Opinion in Microbiology, Vol. 3, Issue 4 https://doi.org/10.1016/S1369-5274(00)00103-X	journal	August 2000
Double-joint PCR: a PCR-based molecular tool for gene manipulations in filamentous fungi Yu, Jae-Hyuk; Hamari, Zsuzsanna; Han, Kap-Hoon Fungal Genetics and Biology, Vol. 41, Issue 11 https://doi.org/10.1016/j.fgb.2004.08.001	journal	November 2004
Novel traits of Trichoderma predicted through the analysis of its secretome Druzhinina, Irina S.; Shelest, Ekaterina; Kubicek, Christian P. FEMS Microbiology Letters, Vol. 337, Issue 1 https://doi.org/10.1111/j.1574-6968.2012.02665.x	journal	September 2012
Global Carbon Utilization Profiles of Wild-Type, Mutant, and Transformant Strains of Hypocrea jecorina Druzhinina, I. S.; Schmoll, M.; Seiboth, B. Applied and Environmental Microbiology, Vol. 72, Issue 3 https://doi.org/10.1128/AEM.72.3.2126-2133.2006	journal	March 2006
Identification of a polyketide synthase gene ( pksP ) of Aspergillus fumigatus involved in conidial pigment biosynthesis and virulence Langfelder, K.; Jahn, Bernhard; Gehringer, Heike Medical Microbiology and Immunology, Vol. 187, Issue 2 https://doi.org/10.1007/s004300050077	journal	October 1998
A polyketide synthase gene required for ochratoxin A biosynthesis in Aspergillus ochraceus O'Callaghan, J.; Caddick, M. X.; Dobson, A. D. W. Microbiology, Vol. 149, Issue 12 https://doi.org/10.1099/mic.0.26619-0	journal	December 2003
Identification of a gene cluster responsible for the biosynthesis of aurofusarin in the Fusarium graminearum species complex Malz, Sascha; Grell, Morten N.; Thrane, Charlotte Fungal Genetics and Biology, Vol. 42, Issue 5 https://doi.org/10.1016/j.fgb.2005.01.010	journal	May 2005
Synthesis of Polymerized Melanin by Cryptococcus neoformans in Infected Rodents Rosas, Ángel L.; Nosanchuk, Joshua D.; Feldmesser, Marta Infection and Immunity, Vol. 68, Issue 5 https://doi.org/10.1128/IAI.68.5.2845-2853.2000	journal	May 2000
Aspergillus fumigatus alb1 encodes naphthopyrone synthase when expressed in Aspergillus oryzae Watanabe, Akira; Fujii, Isao; Tsai, Huei-Fung FEMS Microbiology Letters, Vol. 192, Issue 1 https://doi.org/10.1111/j.1574-6968.2000.tb09356.x	journal	November 2000
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
Global nutrient profiling by Phenotype MicroArrays: a tool complementing genomic and proteomic studies in conidial fungi Atanasova, Lea; Druzhinina, Irina S. Journal of Zhejiang University SCIENCE B, Vol. 11, Issue 3 https://doi.org/10.1631/jzus.B1000007	journal	March 2010
Novel Polyketide Synthase from Nectria haematococca Graziani, Stephane; Vasnier, Christelle; Daboussi, Marie-Josee Applied and Environmental Microbiology, Vol. 70, Issue 5 https://doi.org/10.1128/AEM.70.5.2984-2988.2004	journal	May 2004
The molecular and genetic basis of conidial pigmentation in Aspergillus niger Jørgensen, Thomas R.; Park, Joohae; Arentshorst, Mark Fungal Genetics and Biology, Vol. 48, Issue 5 https://doi.org/10.1016/j.fgb.2011.01.005	journal	May 2011
Putative Polyketide Synthase and Laccase Genes for Biosynthesis of Aurofusarin in Gibberella zeae Kim, J. -E.; Han, K. -H.; Jin, J. Applied and Environmental Microbiology, Vol. 71, Issue 4 https://doi.org/10.1128/AEM.71.4.1701-1708.2005	journal	April 2005
The Developmentally Regulated alb1 Gene ofAspergillus fumigatus: Its Role in Modulation of Conidial Morphology and Virulence Tsai, Huei-Fung; Chang, Yun C.; Washburn, Ronald G. Journal of Bacteriology, Vol. 180, Issue 12 https://doi.org/10.1128/JB.180.12.3031-3038.1998	journal	June 1998
Secondary metabolism in Trichoderma - a genomic perspective Mukherjee, P. K.; Horwitz, B. A.; Kenerley, C. M. Microbiology, Vol. 158, Issue 1 https://doi.org/10.1099/mic.0.053629-0	journal	October 2011
Functional Analyses of Trichoderma reesei LAE1 Reveal Conserved and Contrasting Roles of This Regulator Karimi-Aghcheh, Razieh; Bok, Jin Woo; Phatale, Pallavi A. G3: Genes\|Genomes\|Genetics, Vol. 3, Issue 2 https://doi.org/10.1534/g3.112.005140	journal	February 2013
A novel polyketide biosynthesis gene cluster is involved in fruiting body morphogenesis in the filamentous fungi Sordaria macrospora and Neurospora crassa Nowrousian, Minou Current Genetics, Vol. 55, Issue 2 https://doi.org/10.1007/s00294-009-0236-z	journal	March 2009
Identification of the Viridicatumtoxin and Griseofulvin Gene Clusters from Penicillium aethiopicum Chooi, Yit-Heng; Cacho, Ralph; Tang, Yi Chemistry & Biology, Vol. 17, Issue 5 https://doi.org/10.1016/j.chembiol.2010.03.015	journal	May 2010
Regulation of sexual reproduction in Gibberella zeae ( Fusarium roseum 'Graminearum') by F-2 (Zearalenone) Wolf, J. C.; Mirocha, C. J. Canadian Journal of Microbiology, Vol. 19, Issue 6 https://doi.org/10.1139/m73-117	journal	June 1973
Sexual development in the industrial workhorse Trichoderma reesei Seidl, V.; Seibel, C.; Kubicek, C. P. Proceedings of the National Academy of Sciences, Vol. 106, Issue 33 https://doi.org/10.1073/pnas.0904936106	journal	August 2009
Antioxidant systems in the pathogenic fungi of man and their role in virulence Hamilton, A. J.; Holdom, M. D. Medical Mycology, Vol. 37, Issue 6 https://doi.org/10.1046/j.1365-280X.1999.00208.x	journal	December 1999
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
Biosynthesis and Functions of Melanin inSporothrix schenckii Romero-Martinez, Rafael; Wheeler, Michael; Guerrero-Plata, Antonieta Infection and Immunity, Vol. 68, Issue 6 https://doi.org/10.1128/IAI.68.6.3696-3703.2000	journal	June 2000
Regulation of melanin biosynthesis via the dihydroxynaphthalene pathway is dependent on sexual development in the ascomycete Sordaria macrospora Engh, Ines; Nowrousian, Minou; KÃ¼ck, Ulrich FEMS Microbiology Letters, Vol. 275, Issue 1 https://doi.org/10.1111/j.1574-6968.2007.00867.x	journal	October 2007
Aspergillus niger genomics: Past, present and into the future Baker, Scott E. Medical Mycology, Vol. 44, Issue s1 https://doi.org/10.1080/13693780600921037	journal	January 2006
Histoplasma capsulatum Synthesizes Melanin-Like Pigments In Vitro and during Mammalian Infection Nosanchuk, J. D.; Gomez, B. L.; Youngchim, S. Infection and Immunity, Vol. 70, Issue 9 https://doi.org/10.1128/IAI.70.9.5124-5131.2002	journal	September 2002
The polyketide synthase gene pks4 from Gibberella fujikuroi encodes a key enzyme in the biosynthesis of the red pigment bikaverin Linnemannstöns, Pia; Schulte, Jessica; del Mar Prado, Maria Fungal Genetics and Biology, Vol. 37, Issue 2 https://doi.org/10.1016/S1087-1845(02)00501-7	journal	November 2002
Phenoloxidase and Peroxidase Activities in Zone Lines of Phellinus Weirii Li, C. Y. Mycologia, Vol. 73, Issue 5 https://doi.org/10.1080/00275514.1981.12021412	journal	September 1981
Melanin Riley, P. A. The International Journal of Biochemistry & Cell Biology, Vol. 29, Issue 11 https://doi.org/10.1016/S1357-2725(97)00013-7	journal	November 1997
Isolation and serological analyses of fungal melanins Rosas, Ángel L.; Nosanchuk, Joshua D.; Gómez, Beatriz L. Journal of Immunological Methods, Vol. 244, Issue 1-2 https://doi.org/10.1016/S0022-1759(00)00255-6	journal	October 2000
BREAKING AND ENTERING: Host Penetration by the Fungal Rice Blast Pathogen Magnaporthe grisea Howard, Richard J.; Valent, Barbara Annual Review of Microbiology, Vol. 50, Issue 1 https://doi.org/10.1146/annurev.micro.50.1.491	journal	October 1996
The CRE1 carbon catabolite repressor of the fungus Trichoderma reesei: a master regulator of carbon assimilation Portnoy, Thomas; Margeot, Antoine; Linke, Rita BMC Genomics, Vol. 12, Issue 1 https://doi.org/10.1186/1471-2164-12-269	journal	May 2011
Synthesis and assembly of fungal melanin Eisenman, Helene C.; Casadevall, Arturo Applied Microbiology and Biotechnology, Vol. 93, Issue 3 https://doi.org/10.1007/s00253-011-3777-2	journal	December 2011
Re-identification of Aspergillus nidulans wA gene to code for a polyketide synthase of naphthopyrone Watanabe, Akira; Fujii, Isao; Sankawa, Ushio Tetrahedron Letters, Vol. 40, Issue 1 https://doi.org/10.1016/S0040-4039(98)80027-0	journal	January 1999
Molecular cloning and characterization of an ML-236B (compactin) biosynthetic gene cluster in Penicillium citrinum Abe, Y.; Suzuki, T.; Ono, C. Molecular Genetics and Genomics, Vol. 267, Issue 5 https://doi.org/10.1007/s00438-002-0697-y	journal	July 2002
Evolution and Ecophysiology of the Industrial Producer Hypocrea jecorina (Anamorph Trichoderma reesei) and a New Sympatric Agamospecies Related to It Druzhinina, Irina S.; Komoń-Zelazowska, Monika; Atanasova, Lea PLoS ONE, Vol. 5, Issue 2 https://doi.org/10.1371/journal.pone.0009191	journal	February 2010
Evidence for an Elongation/Reduction/C1-Elimination Pathway in the Biosynthesis of n-Heptane in Xylem of Jeffrey Pine Savage, T. J.; Hristova, M. K.; Croteau, R. Plant Physiology, Vol. 111, Issue 4 https://doi.org/10.1104/pp.111.4.1263	journal	August 1996
Melanisation of Cryptococcus neoformans in human brain tissue Nosanchuk, Joshua D.; Rosas, Angel L.; Lee, Sunhee C. The Lancet, Vol. 355, Issue 9220 https://doi.org/10.1016/S0140-6736(00)02356-4	journal	June 2000
Synthesis of Melanin-Like Pigments by Sporothrix schenckii In Vitro and during Mammalian Infection Morris-Jones, Rachael; Youngchim, Sirida; Gomez, Beatriz L. Infection and Immunity, Vol. 71, Issue 7 https://doi.org/10.1128/IAI.71.7.4026-4033.2003	journal	July 2003
Melanin is an essential component for the integrity of the cell wall of Aspergillus fumigatus conidia Pihet, Marc; Vandeputte, Patrick; Tronchin, Guy BMC Microbiology, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2180-9-177	journal	January 2009
Some chemical and structural features of the conidial wall of Trichoderma viride Benítez, T.; Villa, T. G.; Acha, I. García Canadian Journal of Microbiology, Vol. 22, Issue 2 https://doi.org/10.1139/m76-046	journal	February 1976
Lovastatin biosynthesis in Aspergillus terreus: Characterization of blocked mutants, enzyme activities and a multifunctional polyketide synthase gene Hendrickson, Lee; Ray Davis, C.; Roach, Claudia Chemistry & Biology, Vol. 6, Issue 7 https://doi.org/10.1016/S1074-5521(99)80061-1	journal	July 1999
Colour pigments of Trichoderma harzianum Csiktusnádi Kiss, Gergely; Forgács, Esther; Cserháti, Tibor Journal of Chromatography A, Vol. 896, Issue 1-2 https://doi.org/10.1016/S0021-9673(00)00413-1	journal	October 2000
Melanin and perithecial development in Ophiostoma piliferum Zimmerman, W. C.; Blanchette, R. A.; Burnes, T. A. Mycologia, Vol. 87, Issue 6 https://doi.org/10.1080/00275514.1995.12026606	journal	November 1995
Induction of conidiation by endogenous volatile compounds in Trichoderma spp. NemÄoviÄ, Marek; JakubÃkovÃ¡, Lucia; VÃden, Ivan FEMS Microbiology Letters, Vol. 284, Issue 2 https://doi.org/10.1111/j.1574-6968.2008.01202.x	journal	July 2008
Detection of Melanin-Like Pigments in the Dimorphic Fungal Pathogen Paracoccidioides brasiliensis In Vitro and during Infection Gómez, Beatriz L.; Nosanchuk, Joshua D.; Dı́ez, Soraya Infection and Immunity, Vol. 69, Issue 9 https://doi.org/10.1128/IAI.69.9.5760-5767.2001	journal	September 2001
Aspergillus fumigatus melanins: interference with the host endocytosis pathway and impact on virulence Heinekamp, Thorsten; Thywißen, Andreas; Macheleidt, Juliane Frontiers in Microbiology, Vol. 3 https://doi.org/10.3389/fmicb.2012.00440	journal	January 2013
Biosynthesis of the red pigment bikaverin in Fusarium fujikuroi : genes, their function and regulation Wiemann, Philipp; Willmann, Anita; Straeten, Marcus Molecular Microbiology, Vol. 72, Issue 4 https://doi.org/10.1111/j.1365-2958.2009.06695.x	journal	May 2009
Comparative Analysis of the Genomes of Two Field Isolates of the Rice Blast Fungus Magnaporthe oryzae Xue, Minfeng; Yang, Jun; Li, Zhigang PLoS Genetics, Vol. 8, Issue 8 https://doi.org/10.1371/journal.pgen.1002869	journal	August 2012
Comparative Characterization of Fungal Anthracenone and Naphthacenedione Biosynthetic Pathways Reveals an α-Hydroxylation-Dependent Claisen-like Cyclization Catalyzed by a Dimanganese Thioesterase Li, Yanran; Chooi, Yit-Heng; Sheng, Yuewei Journal of the American Chemical Society, Vol. 133, Issue 39 https://doi.org/10.1021/ja206906d	journal	October 2011
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
Characterization of a polyketide synthase in Aspergillus niger whose product is a precursor for both dihydroxynaphthalene (DHN) melanin and naphtho-γ-pyrone Chiang, Yi-Ming; Meyer, Kristen M.; Praseuth, Michael Fungal Genetics and Biology, Vol. 48, Issue 4 https://doi.org/10.1016/j.fgb.2010.12.001	journal	April 2011
Two Novel Classes of Enzymes Are Required for the Biosynthesis of Aurofusarin in Fusarium graminearum Frandsen, Rasmus J. N.; Schütt, Claes; Lund, Birgitte W. Journal of Biological Chemistry, Vol. 286, Issue 12 https://doi.org/10.1074/jbc.M110.179853	journal	February 2011
Phylogenomic analysis of polyketide synthase-encoding genes in Trichoderma Baker, S. E.; Perrone, G.; Richardson, N. M. Microbiology, Vol. 158, Issue 1 https://doi.org/10.1099/mic.0.053462-0	journal	November 2011
Pentaketide Melanin Biosynthesis in Aspergillus fumigatus Requires Chain-length Shortening of a Heptaketide Precursor Tsai, Huei-Fung; Fujii, Isao; Watanabe, Akira Journal of Biological Chemistry, Vol. 276, Issue 31 https://doi.org/10.1074/jbc.M101998200	journal	May 2001
A versatile transformation system for the cellulolytic filamentous fungus Trichoderma reesei Penttilä, Merja; Nevalainen, Helena; Rättö, Marjaana Gene, Vol. 61, Issue 2, p. 155-164 https://doi.org/10.1016/0378-1119(87)90110-7	journal	January 1987

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