Ecological generalism drives hyperdiversity of secondary metabolite gene clusters in xylarialean endophytes

Franco, Mario E. E.; Wisecaver, Jennifer H.; Arnold, A. Elizabeth; Ju, Yu‐Ming; Slot, Jason C.; Ahrendt, Steven; Moore, Lillian P.; Eastman, Katharine E.; Scott, Kelsey; Konkel, Zachary; Mondo, Stephen J.; Kuo, Alan; Hayes, Richard D.; Haridas, Sajeet; Andreopoulos, Bill; Riley, Robert; LaButti, Kurt; Pangilinan, Jasmyn; Lipzen, Anna; Amirebrahimi, Mojgan; Yan, Juying; Adam, Catherine; Keymanesh, Keykhosrow; Ng, Vivian; Louie, Katherine; Northen, Trent; Drula, Elodie; Henrissat, Bernard; Hsieh, Huei‐Mei; Youens‐Clark, Ken; Lutzoni, François; Miadlikowska, Jolanta; Eastwood, Daniel C.; Hamelin, Richard C.; Grigoriev, Igor V.; U’Ren, Jana M.

doi:10.1111/nph.17873

Title: Ecological generalism drives hyperdiversity of secondary metabolite gene clusters in xylarialean endophytes

Journal Article · Fri Nov 19 00:00:00 UTC 2021 · New Phytologist

DOI: https://doi.org/10.1111/nph.17873 · OSTI ID:1855208

^[1];

^[2];

^[1];

^[3];

^[4];

^[5]; Moore, Lillian P. ^[1];

^[2];

^[4]; Konkel, Zachary ^[4]; Mondo, Stephen J. ^[5]; Kuo, Alan ^[5];

^[5];

^[5]; Andreopoulos, Bill ^[5]; Riley, Robert ^[5];

^[5]; Pangilinan, Jasmyn ^[5];

^[5]; Amirebrahimi, Mojgan ^[5] more »

Univ. of Arizona, Tucson, AZ (United States)
Purdue Univ., West Lafayette, IN (United States)
Academia Sinica, Taipei (Taiwan)
The Ohio State Univ., Columbus, OH (United States)
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Aix‐Marseille Univ. (France); INRAE, Marseille (France)
Technical Univ. of Denmark, Lyngby (Denmark); King Abdulaziz Univ., Jeddah (Saudi Arabia)
Duke Univ., Durham, NC (United States)
Swansea Univ. (United Kingdom)
Univ. of British Columbia, Vancouver, BC (Canada)
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Univ. of California, Berkeley, CA (United States)

Although secondary metabolites are typically associated with competitive or pathogenic interactions, the high bioactivity of endophytic fungi in the Xylariales, coupled with their abundance and broad host ranges spanning all lineages of land plants and lichens, suggests that enhanced secondary metabolism might facilitate symbioses with phylogenetically diverse hosts. Here, we examined secondary metabolite gene clusters (SMGCs) across 96 Xylariales genomes in two clades (Xylariaceae s.l. and Hypoxylaceae), including 88 newly sequenced genomes of endophytes and closely related saprotrophs and pathogens. We paired genomic data with extensive metadata on endophyte hosts and substrates, enabling us to examine genomic factors related to the breadth of symbiotic interactions and ecological roles. All genomes contain hyperabundant SMGCs; however, Xylariaceae have increased numbers of gene duplications, horizontal gene transfers (HGTs) and SMGCs. Enhanced metabolic diversity of endophytes is associated with a greater diversity of hosts and increased capacity for lignocellulose decomposition. Our results suggest that, as host and substrate generalists, Xylariaceae endophytes experience greater selection to diversify SMGCs compared with more ecologically specialised Hypoxylaceae species. Altogether, our results provide new evidence that SMGCs may facilitate symbiosis with phylogenetically diverse hosts, highlighting the importance of microbial symbioses to drive fungal metabolic diversity.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1855208

Journal Information:: New Phytologist, Journal Name: New Phytologist Journal Issue: 3 Vol. 233; ISSN 0028-646X

Publisher:: WileyCopyright Statement

Country of Publication:: United States

Language:: English

References (90)

Host availability drives distributions of fungal endophytes in the imperilled boreal realm U'Ren, Jana; Lutzoni, Francois; Miadlikowska, Jolanta figshare https://doi.org/10.6084/m9.figshare.c.4327772	collection	January 2019
Predicting Secretory Proteins with SignalP Nielsen, Henrik Methods in Molecular Biology https://doi.org/10.1007/978-1-4939-7015-5_6	book	January 2017
Study of endophytic Xylariaceae in Thailand: diversity and taxonomy inferred from rDNA sequence analyses with saprobes forming fruit bodies in the field Okane, Izumi; Toyama, Kyoko; Nakagiri, Akira Mycoscience, Vol. 49, Issue 6 https://doi.org/10.1007/S10267-008-0440-6	journal	December 2008
Diversity in enoyl-acyl carrier protein reductases Massengo-Tiassé, R. P.; Cronan, J. E. Cellular and Molecular Life Sciences, Vol. 66, Issue 9 https://doi.org/10.1007/s00018-009-8704-7	journal	January 2009
Characterization of four endophytic fungi as potential consolidated bioprocessing hosts for conversion of lignocellulose into advanced biofuels Wu, Weihua; Davis, Ryan W.; Tran-Gyamfi, Mary Bao Applied Microbiology and Biotechnology, Vol. 101, Issue 6 https://doi.org/10.1007/s00253-017-8091-1	journal	January 2017
Resurrection and emendation of the Hypoxylaceae, recognised from a multigene phylogeny of the Xylariales Wendt, Lucile; Sir, Esteban Benjamin; Kuhnert, Eric Mycological Progress, Vol. 17, Issue 1-2 https://doi.org/10.1007/s11557-017-1311-3	journal	June 2017
Barrmaelia and Entosordaria in Barrmaeliaceae (fam. nov., Xylariales) and critical notes on Anthostomella-like genera based on multigene phylogenies Voglmayr, Hermann; Friebes, Gernot; Gardiennet, Alain Mycological Progress, Vol. 17, Issue 1-2 https://doi.org/10.1007/s11557-017-1329-6	journal	August 2017
High quality genome sequences of thirteen Hypoxylaceae (Ascomycota) strengthen the phylogenetic family backbone and enable the discovery of new taxa Wibberg, Daniel; Stadler, Marc; Lambert, Christopher Fungal Diversity, Vol. 106, Issue 1 https://doi.org/10.1007/s13225-020-00447-5	journal	May 2020
Fungal Genomics Kuo, Alan; Bushnell, Brian; Grigoriev, Igor V. Fungi, Vol. 70, p. 1-52 https://doi.org/10.1016/B978-0-12-397940-7.00001-X	book	May 2014
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
Distribution of NRPS gene families within the Neotyphodium/Epichloë complex Johnson, Richard; Voisey, Christine; Johnson, Linda Fungal Genetics and Biology, Vol. 44, Issue 11 https://doi.org/10.1016/j.fgb.2007.04.009	journal	November 2007
Host-specificity factors in plant pathogenic fungi Li, Jiming; Cornelissen, Ben; Rep, Martijn Fungal Genetics and Biology, Vol. 144 https://doi.org/10.1016/j.fgb.2020.103447	journal	November 2020
Natural roles of nonribosomal peptide metabolites in fungi Oide, Shinichi; Turgeon, B. Gillian Mycoscience, Vol. 61, Issue 3 https://doi.org/10.1016/j.myc.2020.03.001	journal	May 2020
101 Dothideomycetes genomes: A test case for predicting lifestyles and emergence of pathogens Haridas, S.; Albert, R.; Binder, M. Studies in Mycology, Vol. 96 https://doi.org/10.1016/j.simyco.2020.01.003	journal	June 2020
Acquisition of prokaryotic genes by fungal genomes Marcet-Houben, Marina; Gabaldón, Toni Trends in Genetics, Vol. 26, Issue 1 https://doi.org/10.1016/j.tig.2009.11.007	journal	January 2010
Phylogenetic status of Xylaria subgenus Pseudoxylaria among taxa of the subfamily Xylarioideae (Xylariaceae) and phylogeny of the taxa involved in the subfamily Hsieh, Huei-Mei; Lin, Chun-Ru; Fang, Mei-Jane Molecular Phylogenetics and Evolution, Vol. 54, Issue 3 https://doi.org/10.1016/j.ympev.2009.12.015	journal	March 2010
Contributions of North American endophytes to the phylogeny, ecology, and taxonomy of Xylariaceae (Sordariomycetes, Ascomycota) U’Ren, Jana M.; Miadlikowska, Jolanta; Zimmerman, Naupaka B. Molecular Phylogenetics and Evolution, Vol. 98 https://doi.org/10.1016/j.ympev.2016.02.010	journal	May 2016
Minimum Information about a Biosynthetic Gene cluster Medema, Marnix H.; Kottmann, Renzo; Yilmaz, Pelin Nature Chemical Biology, Vol. 11, Issue 9 https://doi.org/10.1038/nchembio.1890	journal	August 2015
Fast and sensitive protein alignment using DIAMOND Buchfink, Benjamin; Xie, Chao; Huson, Daniel H. Nature Methods, Vol. 12, Issue 1 https://doi.org/10.1038/nmeth.3176	journal	November 2014
ModelFinder: fast model selection for accurate phylogenetic estimates Kalyaanamoorthy, Subha; Minh, Bui Quang; Wong, Thomas K. F. Nature Methods, Vol. 14, Issue 6 https://doi.org/10.1038/nmeth.4285	journal	May 2017
Global analysis of biosynthetic gene clusters reveals vast potential of secondary metabolite production in Penicillium species Nielsen, Jens Christian; Grijseels, Sietske; Prigent, Sylvain Nature Microbiology, Vol. 2, Issue 6 https://doi.org/10.1038/nmicrobiol.2017.44	journal	April 2017
Dimensions of biodiversity in the Earth mycobiome Peay, Kabir G.; Kennedy, Peter G.; Talbot, Jennifer M. Nature Reviews Microbiology, Vol. 14, Issue 7 https://doi.org/10.1038/nrmicro.2016.59	journal	June 2016
Horizontal gene transfer in osmotrophs: playing with public goods Richards, Thomas A.; Talbot, Nicholas J. Nature Reviews Microbiology, Vol. 11, Issue 10 https://doi.org/10.1038/nrmicro3108	journal	September 2013
Specialized plant biochemistry drives gene clustering in fungi Gluck-Thaler, Emile; Slot, Jason C. The ISME Journal, Vol. 12, Issue 7 https://doi.org/10.1038/s41396-018-0075-3	journal	February 2018
Recent progress in biodiversity research on the Xylariales and their secondary metabolism Becker, Kevin; Stadler, Marc The Journal of Antibiotics, Vol. 74, Issue 1 https://doi.org/10.1038/s41429-020-00376-0	journal	October 2020
Large-scale genome sequencing of mycorrhizal fungi provides insights into the early evolution of symbiotic traits Miyauchi, Shingo; Kiss, Enikő; Kuo, Alan Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-18795-w	journal	October 2020
Host availability drives distributions of fungal endophytes in the imperilled boreal realm U’Ren, Jana M.; Lutzoni, François; Miadlikowska, Jolanta Nature Ecology & Evolution, Vol. 3, Issue 10 https://doi.org/10.1038/s41559-019-0975-2	journal	September 2019
The birth, evolution and death of metabolic gene clusters in fungi Rokas, Antonis; Wisecaver, Jennifer H.; Lind, Abigail L. Nature Reviews Microbiology, Vol. 16, Issue 12 https://doi.org/10.1038/s41579-018-0075-3	journal	September 2018
Plant–microbiome interactions: from community assembly to plant health Trivedi, Pankaj; Leach, Jan E.; Tringe, Susannah G. Nature Reviews Microbiology, Vol. 18, Issue 11 https://doi.org/10.1038/s41579-020-0412-1	journal	August 2020
A computational framework to explore large-scale biosynthetic diversity Navarro-Muñoz, Jorge C.; Selem-Mojica, Nelly; Mullowney, Michael W. Nature Chemical Biology, Vol. 16, Issue 1 https://doi.org/10.1038/s41589-019-0400-9	journal	November 2019
Comparative genomics provides insights into the lifestyle and reveals functional heterogeneity of dark septate endophytic fungi Knapp, Dániel G.; Németh, Julianna B.; Barry, Kerrie Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-24686-4	journal	April 2018
The rice endophyte Harpophora oryzae genome reveals evolution from a pathogen to a mutualistic endophyte Xu, Xi-Hui; Su, Zhen-Zhu; Wang, Chen Scientific Reports, Vol. 4, Issue 1 https://doi.org/10.1038/srep05783	journal	July 2014
Functional characterization of salicylate hydroxylase from the fungal endophyte Epichloë festucae Ambrose, Karen V.; Tian, Zipeng; Wang, Yifei Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep10939	journal	June 2015
Horizontally acquired genes in early-diverging pathogenic fungi enable the use of host nucleosides and nucleotides Alexander, William G.; Wisecaver, Jennifer H.; Rokas, Antonis Proceedings of the National Academy of Sciences, Vol. 113, Issue 15 https://doi.org/10.1073/pnas.1517242113	journal	March 2016
An interpreted atlas of biosynthetic gene clusters from 1,000 fungal genomes Robey, Matthew T.; Caesar, Lindsay K.; Drott, Milton T. Proceedings of the National Academy of Sciences, Vol. 118, Issue 19 https://doi.org/10.1073/pnas.2020230118	journal	May 2021
Microevolution in the pansecondary metabolome of Aspergillus flavus and its potential macroevolutionary implications for filamentous fungi Drott, Milton T.; Rush, Tomás A.; Satterlee, Tatum R. Proceedings of the National Academy of Sciences, Vol. 118, Issue 21 https://doi.org/10.1073/pnas.2021683118	journal	May 2021
Phylogenies and the Comparative Method Felsenstein, Joseph The American Naturalist, Vol. 125, Issue 1 https://doi.org/10.1086/284325	journal	January 1985
SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing Bankevich, Anton; Nurk, Sergey; Antipov, Dmitry Journal of Computational Biology, Vol. 19, Issue 5 https://doi.org/10.1089/cmb.2012.0021	journal	May 2012
De novo identification of repeat families in large genomes Price, A. L.; Jones, N. C.; Pevzner, P. A. Bioinformatics, Vol. 21, Issue Suppl 1 https://doi.org/10.1093/bioinformatics/bti1018	journal	June 2005
trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses Capella-Gutierrez, S.; Silla-Martinez, J. M.; Gabaldon, T. Bioinformatics, Vol. 25, Issue 15 https://doi.org/10.1093/bioinformatics/btp348	journal	June 2009
Count: evolutionary analysis of phylogenetic profiles with parsimony and likelihood Csuos, M. Bioinformatics, Vol. 26, Issue 15 https://doi.org/10.1093/bioinformatics/btq315	journal	June 2010
The Architecture of Metabolism Maximizes Biosynthetic Diversity in the Largest Class of Fungi Gluck-Thaler, Emile; Haridas, Sajeet; Binder, Manfred Molecular Biology and Evolution, Vol. 37, Issue 10 https://doi.org/10.1093/molbev/msaa122	journal	May 2020
MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability Katoh, K.; Standley, D. M. Molecular Biology and Evolution, Vol. 30, Issue 4 https://doi.org/10.1093/molbev/mst010	journal	January 2013
IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies Nguyen, Lam-Tung; Schmidt, Heiko A.; von Haeseler, Arndt Molecular Biology and Evolution, Vol. 32, Issue 1 https://doi.org/10.1093/molbev/msu300	journal	November 2014
Dynamic Evolution of Nitric Oxide Detoxifying Flavohemoglobins, a Family of Single-Protein Metabolic Modules in Bacteria and Eukaryotes Wisecaver, Jennifer H.; Alexander, William G.; King, Sean B. Molecular Biology and Evolution, Vol. 33, Issue 8 https://doi.org/10.1093/molbev/msw073	journal	April 2016
Horizontal Transfer of Bacterial Cytolethal Distending Toxin B Genes to Insects Verster, Kirsten I.; Wisecaver, Jennifer H.; Karageorgi, Marianthi Molecular Biology and Evolution, Vol. 36, Issue 10 https://doi.org/10.1093/molbev/msz146	journal	June 2019
From genomics to chemical genomics: new developments in KEGG Kanehisa, M. Nucleic Acids Research, Vol. 34, Issue 90001 https://doi.org/10.1093/nar/gkj102	journal	January 2006
The carbohydrate-active enzymes database (CAZy) in 2013 Lombard, Vincent; Golaconda Ramulu, Hemalatha; Drula, Elodie Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1178	journal	November 2013
MycoCosm portal: gearing up for 1000 fungal genomes Grigoriev, Igor V.; Nikitin, Roman; Haridas, Sajeet Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1183	journal	December 2013
The Transporter Classification Database (TCDB): recent advances Saier, Milton H.; Reddy, Vamsee S.; Tsu, Brian V. Nucleic Acids Research, Vol. 44, Issue D1 https://doi.org/10.1093/nar/gkv1103	journal	November 2015
Twenty years of the MEROPS database of proteolytic enzymes, their substrates and inhibitors Rawlings, Neil D.; Barrett, Alan J.; Finn, Robert Nucleic Acids Research, Vol. 44, Issue D1 https://doi.org/10.1093/nar/gkv1118	journal	November 2015
Reference sequence (RefSeq) database at NCBI: current status, taxonomic expansion, and functional annotation O'Leary, Nuala A.; Wright, Mathew W.; Brister, J. Rodney Nucleic Acids Research, Vol. 44, Issue D1 https://doi.org/10.1093/nar/gkv1189	journal	November 2015
The Gene Ontology Resource: 20 years and still GOing strong Nucleic Acids Research, Vol. 47, Issue D1, p. D330-D338 https://doi.org/10.1093/nar/gky1055	journal	November 2018
InterPro in 2019: improving coverage, classification and access to protein sequence annotations Mitchell, Alex L.; Attwood, Teresa K.; Babbitt, Patricia C. Nucleic Acids Research, Vol. 47, Issue D1 https://doi.org/10.1093/nar/gky1100	journal	November 2018
The Pfam protein families database in 2019 El-Gebali, Sara; Mistry, Jaina; Bateman, Alex Nucleic Acids Research, Vol. 47, Issue D1 https://doi.org/10.1093/nar/gky995	journal	October 2018
Interactive Tree Of Life (iTOL) v4: recent updates and new developments Letunic, Ivica; Bork, Peer Nucleic Acids Research, Vol. 47, Issue W1 https://doi.org/10.1093/nar/gkz239	journal	April 2019
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
A Phylogenetic Estimation of Trophic Transition Networks for Ascomycetous Fungi: Are Lichens Cradles of Symbiotrophic Fungal Diversification? Arnold, A. Elizabeth; Miadlikowska, Jolanta; Higgins, K. Lindsay Systematic Biology, Vol. 58, Issue 3 https://doi.org/10.1093/sysbio/syp001	journal	June 2009
Symbiosis catalyses niche expansion and diversification Joy, Jeffrey B. Proceedings of the Royal Society B: Biological Sciences, Vol. 280, Issue 1756 https://doi.org/10.1098/rspb.2012.2820	journal	April 2013
Fungal evolution: cellular, genomic and metabolic complexity Naranjo‐Ortiz, Miguel A.; Gabaldón, Toni Biological Reviews, Vol. 95, Issue 5 https://doi.org/10.1111/brv.12605	journal	April 2020
Fungal endophytes: diversity and functional roles Rodriguez, R. J.; White Jr, J. F.; Arnold, A. E. New Phytologist, Vol. 182, Issue 2 https://doi.org/10.1111/j.1469-8137.2009.02773.x	journal	February 2009
Fungal adaptation to plant defences through convergent assembly of metabolic modules Gluck‐Thaler, Emile; Vijayakumar, Vinod; Slot, Jason C. Molecular Ecology https://doi.org/10.1111/mec.14943	journal	December 2018
Improved prediction of fungal effector proteins from secretomes with EffectorP 2.0: Prediction of fungal effectors with EffectorP 2.0 Sperschneider, Jana; Dodds, Peter N.; Gardiner, Donald M. Molecular Plant Pathology, Vol. 19, Issue 9 https://doi.org/10.1111/mpp.12682	journal	May 2018
Mutualistic root endophytism is not associated with the reduction of saprotrophic traits and requires a noncompromised plant innate immunity Lahrmann, Urs; Strehmel, Nadine; Langen, Gregor New Phytologist, Vol. 207, Issue 3 https://doi.org/10.1111/nph.13411	journal	April 2015
RNA-based analyses reveal fungal communities structured by a senescence gradient in the moss Dicranum scoparium and the presence of putative multi-trophic fungi Chen, Ko-Hsuan; Liao, Hui-Ling; Arnold, A. Elizabeth New Phytologist, Vol. 218, Issue 4 https://doi.org/10.1111/nph.15092	journal	March 2018
Genome-scale phylogeny and contrasting modes of genome evolution in the fungal phylum Ascomycota Shen, Xing-Xing; Steenwyk, Jacob L.; LaBella, Abigail L. Science Advances, Vol. 6, Issue 45 https://doi.org/10.1126/sciadv.abd0079	journal	November 2020
SidL, an Aspergillus fumigatus Transacetylase Involved in Biosynthesis of the Siderophores Ferricrocin and Hydroxyferricrocin Blatzer, Michael; Schrettl, Markus; Sarg, Bettina Applied and Environmental Microbiology, Vol. 77, Issue 14 https://doi.org/10.1128/AEM.00182-11	journal	July 2011
Role of phyllosphere fungi of forest trees in the development of decomposer fungal communities and decomposition processes of leaf litter Osono, T. Canadian Journal of Microbiology, Vol. 52, Issue 8 https://doi.org/10.1139/w06-023	journal	August 2006
A new Generation of Homology Search Tools Based on Probabilistic Inference Eddy, Sean R. Proceedings of the 20th International Conference, Genome Informatics 2009 https://doi.org/10.1142/9781848165632_0019	conference	March 2012
Hidden Fungi, Emergent Properties: Endophytes and Microbiomes Porras-Alfaro, Andrea; Bayman, Paul Annual Review of Phytopathology, Vol. 49, Issue 1 https://doi.org/10.1146/annurev-phyto-080508-081831	journal	September 2011
The COG database: an updated version includes eukaryotes Tatusov, Roman L.; Fedorova, Natalie D.; Jackson, John D. BMC Bioinformatics, Vol. 4, Article No. 41 https://doi.org/10.1186/1471-2105-4-41	journal	January 2003
Data access for the 1,000 Plants (1KP) project Matasci, Naim; Hung, Ling-Hong; Yan, Zhixiang GigaScience, Vol. 3, Issue 1 https://doi.org/10.1186/2047-217X-3-17	journal	October 2014
Extensive horizontal gene transfers between plant pathogenic fungi Qiu, Huan; Cai, Guohong; Luo, Jing BMC Biology, Vol. 14, Issue 1 https://doi.org/10.1186/s12915-016-0264-3	journal	May 2016
OrthoFinder: phylogenetic orthology inference for comparative genomics Emms, David M.; Kelly, Steven Genome Biology, Vol. 20, Issue 1 https://doi.org/10.1186/s13059-019-1832-y	journal	November 2019
Repbase Update, a database of repetitive elements in eukaryotic genomes Bao, Weidong; Kojima, Kenji K.; Kohany, Oleksiy Mobile DNA, Vol. 6, Issue 1 https://doi.org/10.1186/s13100-015-0041-9	journal	June 2015
CAZymes-based ranking of fungi (CBRF): an interactive web database for identifying fungi with extrinsic plant biomass degrading abilities Kameshwar, Ayyappa Kumar Sista; Ramos, Luiz Pereira; Qin, Wensheng Bioresources and Bioprocessing, Vol. 6, Issue 1 https://doi.org/10.1186/s40643-019-0286-0	journal	December 2019
The Marine Microbial Eukaryote Transcriptome Sequencing Project (MMETSP): Illuminating the Functional Diversity of Eukaryotic Life in the Oceans through Transcriptome Sequencing Keeling, Patrick J.; Burki, Fabien; Wilcox, Heather M. PLoS Biology, Vol. 12, Issue 6 https://doi.org/10.1371/journal.pbio.1001889	journal	June 2014
The Evolution of Fungal Metabolic Pathways Wisecaver, Jennifer H.; Slot, Jason C.; Rokas, Antonis PLoS Genetics, Vol. 10, Issue 12 https://doi.org/10.1371/journal.pgen.1004816	journal	December 2014
Interkingdom Gene Transfer of a Hybrid NPS/PKS from Bacteria to Filamentous Ascomycota Lawrence, Daniel P.; Kroken, Scott; Pryor, Barry M. PLoS ONE, Vol. 6, Issue 11 https://doi.org/10.1371/journal.pone.0028231	journal	November 2011
KinFin: Software for Taxon-Aware Analysis of Clustered Protein Sequences Laetsch, Dominik R.; Blaxter, Mark L. G3: Genes\|Genomes\|Genetics, Vol. 7, Issue 10 https://doi.org/10.1534/g3.117.300233	journal	September 2017
Coniochaeta endophytica sp. nov., a foliar endophyte associated with healthy photosynthetic tissue of Platycladus orientalis (Cupressaceae) Harrington, Alison H.; Olmo-Ruiz, Mariana del; U’Ren, Jana M. Plant and Fungal Systematics, Vol. 64, Issue 1 https://doi.org/10.2478/pfs-2019-0008	journal	July 2019
Host and geographic structure of endophytic and endolichenic fungi at a continental scale U'Ren, Jana M.; Lutzoni, François; Miadlikowska, Jolanta American Journal of Botany, Vol. 99, Issue 5 https://doi.org/10.3732/ajb.1100459	journal	May 2012
Molecular phylogeny of Hypoxylon and closely related genera Hsieh, H. -M.; Ju, Y. -M.; Rogers, J. D. Mycologia, Vol. 97, Issue 4 https://doi.org/10.3852/mycologia.97.4.844	journal	July 2005
Draft genome sequence of the griseofulvin-producing fungus Xylaria flabelliformis strain G536 Mead, Matthew; Raja, Huzefa; Steenwyk, Jacob figshare https://doi.org/10.6084/m9.figshare.8986505	dataset	January 2019
Extensive horizontal gene transfers between plant pathogenic fungi Qiu, Huan; Cai, Guohong; Luo, Jing figshare https://doi.org/10.6084/m9.figshare.c.3616331.v1	collection	January 2016
Signatures of host specialization and a recent transposable element burst in the dynamic one-speed genome of the fungal barley powdery mildew pathogen Frantzeskakis, Lamprinos; Kracher, Barbara; Kusch, Stefan Figshare https://doi.org/10.6084/m9.figshare.c.4108949	collection	January 2018
CAZymes-based ranking of fungi (CBRF): an interactive web database for identifying fungi with extrinsic plant biomass degrading abilities Kameshwar, Ayyappa; Ramos, Luiz; Qin, Wensheng figshare https://doi.org/10.6084/m9.figshare.c.4787886.v1	collection	January 2019
Ecological generalism drives hyperdiversity of secondary metabolite gene clusters in xylarialean endophytes Franco, Mario; Wisecaver, Jennifer; Arnold, A. elizabeth figshare https://doi.org/10.6084/m9.figshare.c.5314025	collection	January 2021
Evidence for loss and reacquisition of alcoholic fermentation in a fructophilic yeast lineage Gonçalves, Carla; Wisecaver, Jennifer H.; Kominek, Jacek eLife, Vol. 7 https://doi.org/10.7554/eLife.33034	journal	April 2018
Diversity, taxonomic composition, and functional aspects of fungal communities in living, senesced, and fallen leaves at five sites across North America U’Ren, Jana M.; Arnold, A. Elizabeth PeerJ, Vol. 4 https://doi.org/10.7717/peerj.2768	journal	January 2016

Similar Records

Uncovering secondary metabolite evolution and biosynthesis using gene cluster networks and genetic dereplication

Journal Article · Tue Dec 18 00:00:00 UTC 2018 · Scientific Reports · OSTI ID:1619562

Theobald, Sebastian; Vesth, Tammi C.; Rendsvig, Jakob Kræmmer; +8 more

Expanding the genomic encyclopedia of Actinobacteria with 824 isolate reference genomes

Journal Article · Fri Nov 11 00:00:00 UTC 2022 · Cell Genomics · OSTI ID:2475937

Seshadri, Rekha; Roux, Simon; Huber, Katharina J.; +37 more

Holo-Omics disentangle drought response and biotic interactions among plant, endophyte and pathogen

Journal Article · Mon Jun 30 04:00:00 UTC 2025 · New Phytologist · OSTI ID:2572964

Chen, Peilin; Yu, Qingyi; Wang, Cong; +20 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Ascomycota
Xylariales
endophyte
plant–fungal interactions
saprotroph
specialised metabolism
symbiosis
trophic mode

Title: Ecological generalism drives hyperdiversity of secondary metabolite gene clusters in xylarialean endophytes

Citation Formats

References (90)

Similar Records

Related Subjects