A Sesquiterpene Synthase from the Endophytic Fungus Serendipita indica Catalyzes Formation of Viridiflorol

Ntana, Fani; Bhat, Wajid W.; Johnson, Sean R.; Jørgensen, Hans J. L.; Collinge, David B.; Jensen, Birgit; Hamberger, Björn

doi:10.3390/biom11060898

A Sesquiterpene Synthase from the Endophytic Fungus Serendipita indica Catalyzes Formation of Viridiflorol

Journal Article · Wed Jun 16 00:00:00 EDT 2021 · Biomolecules

DOI:https://doi.org/10.3390/biom11060898· OSTI ID:1797533

Ntana, Fani; ; ; ; Collinge, David B.; ; Hamberger, Björn

Interactions between plant-associated fungi and their hosts are characterized by a continuous crosstalk of chemical molecules. Specialized metabolites are often produced during these associations and play important roles in the symbiosis between the plant and the fungus, as well as in the establishment of additional interactions between the symbionts and other organisms present in the niche. Serendipita indica, a root endophytic fungus from the phylum Basidiomycota, is able to colonize a wide range of plant species, conferring many benefits to its hosts. The genome of S. indica possesses only few genes predicted to be involved in specialized metabolite biosynthesis, including a putative terpenoid synthase gene (SiTPS). In our experimental setup, SiTPS expression was upregulated when the fungus colonized tomato roots compared to its expression in fungal biomass growing on synthetic medium. Heterologous expression of SiTPS in Escherichia coli showed that the produced protein catalyzes the synthesis of a few sesquiterpenoids, with the alcohol viridiflorol being the main product. To investigate the role of SiTPS in the plant-endophyte interaction, an SiTPS-over-expressing mutant line was created and assessed for its ability to colonize tomato roots. Although overexpression of SiTPS did not lead to improved fungal colonization ability, an in vitro growth-inhibition assay showed that viridiflorol has antifungal properties. Addition of viridiflorol to the culture medium inhibited the germination of spores from a phytopathogenic fungus, indicating that SiTPS and its products could provide S. indica with a competitive advantage over other plant-associated fungi during root colonization.

View Journal Article

Research Organization:: Univ. of Wisconsin, Madison, WI (United States)

Sponsoring Organization:: European Research Council (ERC); National Science Foundation (NSF); USDOE; USDOE Office of Science (SC)

Grant/Contract Number:: FC02-07ER64494; SC0018409

OSTI ID:: 1797533

Alternate ID(s):: OSTI ID: 1852645

Journal Information:: Biomolecules, Journal Name: Biomolecules Journal Issue: 6 Vol. 11; ISSN 2218-273X; ISSN BIOMHC

Publisher:: MDPI AGCopyright Statement

Country of Publication:: Switzerland

Language:: English

References (62)

Sesquiterpene Synthases Cop4 and Cop6 from Coprinus cinereus: Catalytic Promiscuity and Cyclization of Farnesyl Pyrophosphate Geometric Isomers Lopez-Gallego, Fernando; Agger, Sean A.; Abate-Pella, Daniel ChemBioChem, Vol. 11, Issue 8 https://doi.org/10.1002/cbic.200900671	journal	April 2010
Mushroom Hunting by Using Bioinformatics: Application of a Predictive Framework Facilitates the Selective Identification of Sesquiterpene Synthases in Basidiomycota Quin, Maureen B.; Flynn, Christopher M.; Wawrzyn, Grayson T. ChemBioChem, Vol. 14, Issue 18 https://doi.org/10.1002/cbic.201300349	journal	October 2013
Moonlighting Metals: Insights into Regulation of Cyclization Pathways in Fungal Δ ⁶ -Protoilludene Sesquiterpene Synthases Quin, Maureen B.; Michel, Stephen N.; Schmidt-Dannert, Claudia ChemBioChem, Vol. 16, Issue 15 https://doi.org/10.1002/cbic.201500308	journal	September 2015
Headspace solid-phase microextraction with gas chromatography and mass spectrometry in the investigation of volatile organic compounds in an ectomycorrhizae synthesis system: SPME-GC/MS of VOCs in an ectomycorrhizae synthesis system Menotta, Michele; Gioacchini, Anna M.; Amicucci, Antonella Rapid Communications in Mass Spectrometry, Vol. 18, Issue 2 https://doi.org/10.1002/rcm.1314	journal	December 2003
Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method Livak, Kenneth J.; Schmittgen, Thomas D. Methods, Vol. 25, Issue 4 https://doi.org/10.1006/meth.2001.1262	journal	December 2001
Increasing diterpene yield with a modular metabolic engineering system in E. coli: comparison of MEV and MEP isoprenoid precursor pathway engineering Morrone, Dana; Lowry, Luke; Determan, Mara K. Applied Microbiology and Biotechnology, Vol. 85, Issue 6 https://doi.org/10.1007/s00253-009-2219-x	journal	September 2009
Belowground volatiles facilitate interactions between plant roots and soil organisms Wenke, Katrin; Kai, Marco; Piechulla, Birgit Planta, Vol. 231, Issue 3 https://doi.org/10.1007/s00425-009-1076-2	journal	December 2009
Impact of Piriformospora indica on tomato growth and on interaction with fungal and viral pathogens Fakhro, Ahmad; Andrade-Linares, Diana Rocío; von Bargen, Susanne Mycorrhiza, Vol. 20, Issue 3 https://doi.org/10.1007/s00572-009-0279-5	journal	September 2009
Induction of root colonization by Piriformospora indica leads to enhanced asiaticoside production in Centella asiatica Satheesan, Jisha; Narayanan, Anith K.; Sakunthala, Manjula Mycorrhiza, Vol. 22, Issue 3 https://doi.org/10.1007/s00572-011-0394-y	journal	June 2011
The root endophytic fungus Serendipita indica improves resistance of Banana to Fusarium oxysporum f. sp. cubense tropical race 4 Cheng, Chunzhen; Li, Dan; Qi, Quan European Journal of Plant Pathology, Vol. 156, Issue 1 https://doi.org/10.1007/s10658-019-01863-3	journal	October 2019
Changes in Volatile Production During the Course of Fungal Mycelial Interactions Between Hypholoma fasciculare and Resinicium bicolor Hynes, Juliet; Müller, Carsten T.; Jones, T. Hefin Journal of Chemical Ecology, Vol. 33, Issue 1 https://doi.org/10.1007/s10886-006-9209-6	journal	December 2006
Marked enhancement in the artemisinin content and biomass productivity in Artemisia annua L. shoots co-cultivated with Piriformospora indica Sharma, Gaurav; Agrawal, Veena World Journal of Microbiology and Biotechnology, Vol. 29, Issue 6 https://doi.org/10.1007/s11274-013-1263-y	journal	January 2013
Abietic acid, and activator of basidiospore germination in ectomycorrhizal species of the genus Suillus (Boletaceae) Fries, Nils; Serck-Hanssen, Klaus; Dimberg, Lena Häll Experimental Mycology, Vol. 11, Issue 4 https://doi.org/10.1016/0147-5975(87)90024-7	journal	December 1987
The synthesis of mono- and dihydroxy aromadendrane sesquiterpenes, starting from natural (+)-aromadendrene-III Gijsen, Harrie J. M.; Wijnberg, Joannes B. P. A.; Stork, Gerrit A. Tetrahedron, Vol. 48, Issue 12 https://doi.org/10.1016/S0040-4020(01)88765-2	journal	March 1992
Draft Genome of Omphalotus olearius Provides a Predictive Framework for Sesquiterpenoid Natural Product Biosynthesis in Basidiomycota Wawrzyn, Grayson T.; Quin, Maureen B.; Choudhary, Swati Chemistry & Biology, Vol. 19, Issue 6 https://doi.org/10.1016/j.chembiol.2012.05.012	journal	June 2012
Piriformospora indica confers drought tolerance on Zea mays L. through enhancement of antioxidant activity and expression of drought-related genes Xu, Le; Wang, Aiai; Wang, Jun The Crop Journal, Vol. 5, Issue 3 https://doi.org/10.1016/j.cj.2016.10.002	journal	June 2017
Karyotype analysis, genome organization, and stable genetic transformation of the root colonizing fungus Piriformospora indica Zuccaro, Alga; Basiewicz, Magdalena; Zurawska, Magdalena Fungal Genetics and Biology, Vol. 46, Issue 8 https://doi.org/10.1016/j.fgb.2009.03.009	journal	August 2009
A putative terpene cyclase, vir4, is responsible for the biosynthesis of volatile terpene compounds in the biocontrol fungus Trichoderma virens Crutcher, Frankie K.; Parich, Alexandra; Schuhmacher, Rainer Fungal Genetics and Biology, Vol. 56 https://doi.org/10.1016/j.fgb.2013.05.003	journal	July 2013
Expression of the Fusarium graminearum terpenome and involvement of the endoplasmic reticulum-derived toxisome Flynn, Christopher M.; Broz, Karen; Jonkers, Wilfried Fungal Genetics and Biology, Vol. 124 https://doi.org/10.1016/j.fgb.2019.01.006	journal	March 2019
Anti-inflammatory, antioxidant and anti- Mycobacterium tuberculosis activity of viridiflorol: The major constituent of Allophylus edulis (A. St.-Hil., A. Juss. & Cambess.) Radlk. Trevizan, Lucas Noboru Fatori; Nascimento, Kamilla Felipe do; Santos, Joyce Alencar Journal of Ethnopharmacology, Vol. 192 https://doi.org/10.1016/j.jep.2016.08.053	journal	November 2016
Piriformospora indica confers drought tolerance in Chinese cabbage leaves by stimulating antioxidant enzymes, the expression of drought-related genes and the plastid-localized CAS protein Sun, Chao; Johnson, Joy M.; Cai, Daguang Journal of Plant Physiology, Vol. 167, Issue 12 https://doi.org/10.1016/j.jplph.2010.02.013	journal	August 2010
Bioactivity guided isolation of antifungal compounds from the liverwort Bazzania trilobata (L.) S.F. Gray Scher, Jochen M.; Speakman, John-Bryan; Zapp, Josef Phytochemistry, Vol. 65, Issue 18 https://doi.org/10.1016/j.phytochem.2004.05.013	journal	September 2004
The molecular basis of host plant selection in Melaleuca quinquenervia by a successful biological control agent Padovan, Amanda; Keszei, Andras; Köllner, Tobias G. Phytochemistry, Vol. 71, Issue 11-12 https://doi.org/10.1016/j.phytochem.2010.05.013	journal	August 2010
Systematic engineering for high-yield production of viridiflorol and amorphadiene in auxotrophic Escherichia coli Shukal, Sudha; Chen, Xixian; Zhang, Congqiang Metabolic Engineering, Vol. 55 https://doi.org/10.1016/j.ymben.2019.07.007	journal	September 2019
Is a 1,4-Alkyl Shift Involved in the Biosynthesis of Ledol and Viridiflorol? Hong, Young J.; Tantillo, Dean J. The Journal of Organic Chemistry, Vol. 82, Issue 7 https://doi.org/10.1021/acs.joc.7b00187	journal	March 2017
Structural Biology and Chemistry of the Terpenoid Cyclases Christianson, David W. Chemical Reviews, Vol. 106, Issue 8 https://doi.org/10.1021/cr050286w	journal	August 2006
A Modular Approach for Facile Biosynthesis of Labdane-Related Diterpenes Cyr, Anthony; Wilderman, P. Ross; Determan, Mara Journal of the American Chemical Society, Vol. 129, Issue 21 https://doi.org/10.1021/ja071158n	journal	May 2007
The function of terpene natural products in the natural world Gershenzon, Jonathan; Dudareva, Natalia Nature Chemical Biology, Vol. 3, Issue 7 https://doi.org/10.1038/nchembio.2007.5	journal	June 2007
The fungal-specific β-glucan-binding lectin FGB1 alters cell-wall composition and suppresses glucan-triggered immunity in plants Wawra, Stephan; Fesel, Philipp; Widmer, Heidi Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms13188	journal	October 2016
Analyzing real-time PCR data by the comparative CT method Schmittgen, Thomas D.; Livak, Kenneth J. Nature Protocols, Vol. 3, Issue 6 https://doi.org/10.1038/nprot.2008.73	journal	June 2008
Transcriptional responses of soybean roots to colonization with the root endophytic fungus Piriformospora indica reveals altered phenylpropanoid and secondary metabolism Bajaj, Ruchika; Huang, Yinyin; Gebrechristos, Sebhat Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-26809-3	journal	July 2018
Fungal natural products in research and development Schueffler, Anja; Anke, Timm Nat. Prod. Rep., Vol. 31, Issue 10 https://doi.org/10.1039/C4NP00060A	journal	January 2014
The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield Waller, F.; Achatz, B.; Baltruschat, H. Proceedings of the National Academy of Sciences, Vol. 102, Issue 38 https://doi.org/10.1073/pnas.0504423102	journal	September 2005
Cloning and Characterization of an Armillaria gallica cDNA Encoding Protoilludene Synthase, Which Catalyzes the First Committed Step in the Synthesis of Antimicrobial Melleolides Engels, Benedikt; Heinig, Uwe; Grothe, Torsten Journal of Biological Chemistry, Vol. 286, Issue 9 https://doi.org/10.1074/jbc.M110.165845	journal	March 2011
A database-driven approach identifies additional diterpene synthase activities in the mint family (Lamiaceae) Johnson, Sean R.; Bhat, Wajid Waheed; Bibik, Jacob Journal of Biological Chemistry, Vol. 294, Issue 4 https://doi.org/10.1074/jbc.RA118.006025	journal	November 2018
MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms Kumar, Sudhir; Stecher, Glen; Li, Michael Molecular Biology and Evolution, Vol. 35, Issue 6 https://doi.org/10.1093/molbev/msy096	journal	May 2018
antiSMASH 5.0: updates to the secondary metabolite genome mining pipeline Blin, Kai; Shaw, Simon; Steinke, Katharina Nucleic Acids Research, Vol. 47, Issue W1 https://doi.org/10.1093/nar/gkz310	journal	April 2019
Systemic Resistance in Arabidopsis Conferred by the Mycorrhizal Fungus Piriformospora indica Requires Jasmonic Acid Signaling and the Cytoplasmic Function of NPR1 Stein, Elke; Molitor, Alexandra; Kogel, Karl-Heinz Plant and Cell Physiology, Vol. 49, Issue 11 https://doi.org/10.1093/pcp/pcn147	journal	October 2008
Growth Promotion of Chinese Cabbage and Arabidopsis by Piriformospora indica Is Not Stimulated by Mycelium-Synthesized Auxin Lee, Yin-Chen; Johnson, Joy Michal; Chien, Ching-Te Molecular Plant-Microbe Interactions®, Vol. 24, Issue 4 https://doi.org/10.1094/MPMI-05-10-0110	journal	April 2011
Opprimo ergo sum —Evasion and Suppression in the Root Endophytic Fungus Piriformospora indica Lahrmann, Urs; Zuccaro, Alga Molecular Plant-Microbe Interactions®, Vol. 25, Issue 6 https://doi.org/10.1094/MPMI-11-11-0291	journal	June 2012
The Role of Auxins and Cytokinins in the Mutualistic Interaction Between Arabidopsis and Piriformospora indica Vadassery, Jyothilakshmi; Ritter, Claudia; Venus, Yvonne Molecular Plant-Microbe Interactions®, Vol. 21, Issue 10 https://doi.org/10.1094/MPMI-21-10-1371	journal	October 2008
Broad-Spectrum Suppression of Innate Immunity Is Required for Colonization of Arabidopsis Roots by the Fungus Piriformospora indica Jacobs, Sophie; Zechmann, Bernd; Molitor, Alexandra Plant Physiology, Vol. 156, Issue 2 https://doi.org/10.1104/pp.111.176446	journal	April 2011
Diversity of sesquiterpene synthases in the basidiomycete Coprinus cinereus Agger, Sean; Lopez-Gallego, Fernando; Schmidt-Dannert, Claudia Molecular Microbiology, Vol. 72, Issue 5 https://doi.org/10.1111/j.1365-2958.2009.06717.x	journal	June 2009
Manipulation of plant innate immunity and gibberellin as factor of compatibility in the mutualistic association of barley roots with Piriformospora indica Schäfer, Patrick; Pfiffi, Stefanie; Voll, Lars M. The Plant Journal, Vol. 59, Issue 3 https://doi.org/10.1111/j.1365-313X.2009.03887.x	journal	August 2009
Piriformospora indica affects plant growth by auxin production Sirrenberg, Anke; Göbel, Cornelia; Grond, Stephanie Physiologia Plantarum, Vol. 131, Issue 4 https://doi.org/10.1111/j.1399-3054.2007.00983.x	journal	December 2007
Indole derivative production by the root endophyte Piriformospora indica is not required for growth promotion but for biotrophic colonization of barley roots Hilbert, Magdalena; Voll, Lars M.; Ding, Yi New Phytologist, Vol. 196, Issue 2 https://doi.org/10.1111/j.1469-8137.2012.04275.x	journal	August 2012
Promiscuous terpene synthases from Prunella vulgaris highlight the importance of substrate and compartment switching in terpene synthase evolution Johnson, Sean R.; Bhat, Wajid Waheed; Sadre, Radin New Phytologist, Vol. 223, Issue 1 https://doi.org/10.1111/nph.15778	journal	April 2019
The inconspicuous gatekeeper: endophytic Serendipita vermifera acts as extended plant protection barrier in the rhizosphere Sarkar, Debika; Rovenich, Hanna; Jeena, Ganga New Phytologist, Vol. 224, Issue 2 https://doi.org/10.1111/nph.15904	journal	June 2019
Sesquiterpene Synthase–3-Hydroxy-3-Methylglutaryl Coenzyme A Synthase Fusion Protein Responsible for Hirsutene Biosynthesis in Stereum hirsutum Flynn, Christopher M.; Schmidt-Dannert, Claudia Applied and Environmental Microbiology, Vol. 84, Issue 11 https://doi.org/10.1128/AEM.00036-18	journal	June 2018
Selectivity of Fungal Sesquiterpene Synthases: Role of the Active Site's H-1α Loop in Catalysis LÃ¯Â¿Â½pez-Gallego, Fernando; Wawrzyn, GraysonT.; Schmidt-Dannert, Claudia Applied and Environmental Microbiology, Vol. 76, Issue 23 https://doi.org/10.1128/AEM.01811-10	journal	October 2010
Piriformospora indica , a Cultivable Plant-Growth-Promoting Root Endophyte Varma, Ajit; Verma, Savita Applied and Environmental Microbiology, Vol. 65, Issue 6, p. 2741-2744 https://doi.org/10.1128/AEM.65.6.2741-2744.1999	journal	June 1999
Growth improvement of Lolium multiflorum Lam. induced by seed inoculation with fungus suspension of Xerocomus badius and Serendipita indica Liu, Binghua; Liu, Xinghong; Liu, Fangchun AMB Express, Vol. 9, Issue 1 https://doi.org/10.1186/s13568-019-0865-7	journal	September 2019
Rapid Discovery and Functional Characterization of Terpene Synthases from Four Endophytic Xylariaceae Wu, Weihua; Tran, William; Taatjes, Craig A. PLOS ONE, Vol. 11, Issue 2 https://doi.org/10.1371/journal.pone.0146983	journal	February 2016
Endophytic Life Strategies Decoded by Genome and Transcriptome Analyses of the Mutualistic Root Symbiont Piriformospora indica Zuccaro, Alga; Lahrmann, Urs; Güldener, Ulrich PLoS Pathogens, Vol. 7, Issue 10 https://doi.org/10.1371/journal.ppat.1002290	journal	October 2011
Serendipita indica E5′ NT modulates extracellular nucleotide levels in the plant apoplast and affects fungal colonization Nizam, Shadab; Qiang, Xiaoyu; Wawra, Stephan EMBO reports, Vol. 20, Issue 2 https://doi.org/10.15252/embr.201847430	journal	February 2019
The Piriformospora indica effector PIIN_08944 promotes the mutualistic Sebacinalean symbiosis Akum, Fidele N.; Steinbrenner, Jens; Biedenkopf, Dagmar Frontiers in Plant Science, Vol. 6 https://doi.org/10.3389/fpls.2015.00906	journal	October 2015
Chemical Composition and Bioactivity of Essential Oil from Blepharocalyx salicifolius Furtado, Fabiana; Borges, Bruna; Teixeira, Thaise International Journal of Molecular Sciences, Vol. 19, Issue 1 https://doi.org/10.3390/ijms19010033	journal	January 2018
Phytochemical Study of the Ecuadorian Species Lepechinia mutica (Benth.) Epling and High Antifungal Activity of Carnosol against Pyricularia oryzae Ramírez, Jorge; Gilardoni, Gianluca; Ramón, Erika Pharmaceuticals, Vol. 11, Issue 2 https://doi.org/10.3390/ph11020033	journal	April 2018
The Fungi: 1, 2, 3 … 5.1 million species? Blackwell, Meredith American Journal of Botany, Vol. 98, Issue 3 https://doi.org/10.3732/ajb.1000298	journal	March 2011
Chemical profile and antifungal potential of essential oils from leaves and flowers of Salvia algeriensis (Desf.): A comparative study Medjahed, Fatiha; Merouane, Abdelaziz; Saadi, Abdelkader Chilean journal of agricultural research, Vol. 76, Issue 2 https://doi.org/10.4067/S0718-58392016000200009	journal	January 2016
The root endophyte fungus Piriformospora indica leads to early flowering, higher biomass and altered secondary metabolites of the medicinal plant, Coleus forskohlii Das, Aparajita; Kamal, Shwet; Shakil, Najam Akhtar Plant Signaling & Behavior, Vol. 7, Issue 1 https://doi.org/10.4161/psb.7.1.18472	journal	January 2012
Muscodor strobelii, a new endophytic species from South India Meshram, Vineet; Saxena, Sanjai; Kapoor, Neha Mycotaxon, Vol. 128, Issue 1 https://doi.org/10.5248/128.93	journal	August 2014

Similar Records

Transcriptomics reveal a mechanism of niche defense: two beneficial root endophytes deploy an antimicrobial GH18-CBM5 chitinase to protect their hosts

Journal Article · Mon Sep 02 20:00:00 EDT 2024 · New Phytologist · OSTI ID:2477365

A putative cyclin, SiPHO80 from root endophytic fungus Serendipita indica regulates phosphate homeostasis, salinity and heavy metal toxicity tolerance

Journal Article · Fri Dec 14 23:00:00 EST 2018 · Biochemical and Biophysical Research Communications · OSTI ID:23107879

Related Subjects

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
59 BASIC BIOLOGICAL SCIENCES
Basidiomycota
Biochemistry & Molecular Biology
Piriformospora indica
antifungal
endophyte
sesquiterpenoid
terpene synthase
viridiflorol

A Sesquiterpene Synthase from the Endophytic Fungus Serendipita indica Catalyzes Formation of Viridiflorol

Citation Formats

References (62)

Similar Records

Related Subjects