Skip to main content
U.S. Department of Energy
Office of Scientific and Technical Information

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

Journal Article · · New Phytologist
DOI:https://doi.org/10.1111/nph.17873· OSTI ID:1855208
 [1];  [2];  [1];  [3];  [4];  [5];  [1];  [2];  [4];  [4];  [5];  [5];  [5];  [5];  [5];  [5];  [5];  [5];  [5];  [5] more »;  [5];  [5];  [5];  [5];  [5];  [5];  [6];  [7];  [3];  [1];  [8];  [8];  [9];  [10];  [11];  [1] « less
  1. Univ. of Arizona, Tucson, AZ (United States)
  2. Purdue Univ., West Lafayette, IN (United States)
  3. Academia Sinica, Taipei (Taiwan)
  4. The Ohio State Univ., Columbus, OH (United States)
  5. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  6. Aix‐Marseille Univ. (France); INRAE, Marseille (France)
  7. Technical Univ. of Denmark, Lyngby (Denmark); King Abdulaziz Univ., Jeddah (Saudi Arabia)
  8. Duke Univ., Durham, NC (United States)
  9. Swansea Univ. (United Kingdom)
  10. Univ. of British Columbia, Vancouver, BC (Canada)
  11. 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.
Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
1855208
Alternate ID(s):
OSTI ID: 1834427
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 collection January 2019
Predicting Secretory Proteins with SignalP 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 journal December 2008
Diversity in enoyl-acyl carrier protein reductases journal January 2009
Characterization of four endophytic fungi as potential consolidated bioprocessing hosts for conversion of lignocellulose into advanced biofuels journal January 2017
Resurrection and emendation of the Hypoxylaceae, recognised from a multigene phylogeny of the Xylariales journal June 2017
Barrmaelia and Entosordaria in Barrmaeliaceae (fam. nov., Xylariales) and critical notes on Anthostomella-like genera based on multigene phylogenies journal August 2017
High quality genome sequences of thirteen Hypoxylaceae (Ascomycota) strengthen the phylogenetic family backbone and enable the discovery of new taxa journal May 2020
Fungal Genomics book May 2014
Identification of the Viridicatumtoxin and Griseofulvin Gene Clusters from Penicillium aethiopicum journal May 2010
Distribution of NRPS gene families within the Neotyphodium/Epichloë complex journal November 2007
Host-specificity factors in plant pathogenic fungi journal November 2020
Natural roles of nonribosomal peptide metabolites in fungi journal May 2020
101 Dothideomycetes genomes: A test case for predicting lifestyles and emergence of pathogens journal June 2020
Acquisition of prokaryotic genes by fungal genomes 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 journal March 2010
Contributions of North American endophytes to the phylogeny, ecology, and taxonomy of Xylariaceae (Sordariomycetes, Ascomycota) journal May 2016
Minimum Information about a Biosynthetic Gene cluster journal August 2015
Fast and sensitive protein alignment using DIAMOND journal November 2014
ModelFinder: fast model selection for accurate phylogenetic estimates journal May 2017
Global analysis of biosynthetic gene clusters reveals vast potential of secondary metabolite production in Penicillium species journal April 2017
Dimensions of biodiversity in the Earth mycobiome journal June 2016
Horizontal gene transfer in osmotrophs: playing with public goods journal September 2013
Specialized plant biochemistry drives gene clustering in fungi journal February 2018
Recent progress in biodiversity research on the Xylariales and their secondary metabolism journal October 2020
Large-scale genome sequencing of mycorrhizal fungi provides insights into the early evolution of symbiotic traits journal October 2020
Host availability drives distributions of fungal endophytes in the imperilled boreal realm journal September 2019
The birth, evolution and death of metabolic gene clusters in fungi journal September 2018
Plant–microbiome interactions: from community assembly to plant health journal August 2020
A computational framework to explore large-scale biosynthetic diversity journal November 2019
Comparative genomics provides insights into the lifestyle and reveals functional heterogeneity of dark septate endophytic fungi journal April 2018
The rice endophyte Harpophora oryzae genome reveals evolution from a pathogen to a mutualistic endophyte journal July 2014
Functional characterization of salicylate hydroxylase from the fungal endophyte Epichloë festucae journal June 2015
Horizontally acquired genes in early-diverging pathogenic fungi enable the use of host nucleosides and nucleotides journal March 2016
An interpreted atlas of biosynthetic gene clusters from 1,000 fungal genomes journal May 2021
Microevolution in the pansecondary metabolome of Aspergillus flavus and its potential macroevolutionary implications for filamentous fungi journal May 2021
Phylogenies and the Comparative Method journal January 1985
SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing journal May 2012
De novo identification of repeat families in large genomes journal June 2005
trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses journal June 2009
Count: evolutionary analysis of phylogenetic profiles with parsimony and likelihood journal June 2010
The Architecture of Metabolism Maximizes Biosynthetic Diversity in the Largest Class of Fungi journal May 2020
MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability journal January 2013
IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies journal November 2014
Dynamic Evolution of Nitric Oxide Detoxifying Flavohemoglobins, a Family of Single-Protein Metabolic Modules in Bacteria and Eukaryotes journal April 2016
Horizontal Transfer of Bacterial Cytolethal Distending Toxin B Genes to Insects journal June 2019
From genomics to chemical genomics: new developments in KEGG journal January 2006
The carbohydrate-active enzymes database (CAZy) in 2013 journal November 2013
MycoCosm portal: gearing up for 1000 fungal genomes journal December 2013
The Transporter Classification Database (TCDB): recent advances journal November 2015
Twenty years of the MEROPS database of proteolytic enzymes, their substrates and inhibitors journal November 2015
Reference sequence (RefSeq) database at NCBI: current status, taxonomic expansion, and functional annotation journal November 2015
The Gene Ontology Resource: 20 years and still GOing strong journal November 2018
InterPro in 2019: improving coverage, classification and access to protein sequence annotations journal November 2018
The Pfam protein families database in 2019 journal October 2018
Interactive Tree Of Life (iTOL) v4: recent updates and new developments journal April 2019
antiSMASH 5.0: updates to the secondary metabolite genome mining pipeline journal April 2019
A Phylogenetic Estimation of Trophic Transition Networks for Ascomycetous Fungi: Are Lichens Cradles of Symbiotrophic Fungal Diversification? journal June 2009
Symbiosis catalyses niche expansion and diversification journal April 2013
Fungal evolution: cellular, genomic and metabolic complexity journal April 2020
Fungal endophytes: diversity and functional roles journal February 2009
Fungal adaptation to plant defences through convergent assembly of metabolic modules journal December 2018
Improved prediction of fungal effector proteins from secretomes with EffectorP 2.0: Prediction of fungal effectors with EffectorP 2.0 journal May 2018
Mutualistic root endophytism is not associated with the reduction of saprotrophic traits and requires a noncompromised plant innate immunity 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 journal March 2018
Genome-scale phylogeny and contrasting modes of genome evolution in the fungal phylum Ascomycota journal November 2020
SidL, an Aspergillus fumigatus Transacetylase Involved in Biosynthesis of the Siderophores Ferricrocin and Hydroxyferricrocin journal July 2011
Role of phyllosphere fungi of forest trees in the development of decomposer fungal communities and decomposition processes of leaf litter journal August 2006
A new Generation of Homology Search Tools Based on Probabilistic Inference conference March 2012
Hidden Fungi, Emergent Properties: Endophytes and Microbiomes journal September 2011
The COG database: an updated version includes eukaryotes journal January 2003
Data access for the 1,000 Plants (1KP) project journal October 2014
Extensive horizontal gene transfers between plant pathogenic fungi journal May 2016
OrthoFinder: phylogenetic orthology inference for comparative genomics journal November 2019
Repbase Update, a database of repetitive elements in eukaryotic genomes journal June 2015
CAZymes-based ranking of fungi (CBRF): an interactive web database for identifying fungi with extrinsic plant biomass degrading abilities journal December 2019
The Marine Microbial Eukaryote Transcriptome Sequencing Project (MMETSP): Illuminating the Functional Diversity of Eukaryotic Life in the Oceans through Transcriptome Sequencing journal June 2014
The Evolution of Fungal Metabolic Pathways journal December 2014
Interkingdom Gene Transfer of a Hybrid NPS/PKS from Bacteria to Filamentous Ascomycota journal November 2011
KinFin: Software for Taxon-Aware Analysis of Clustered Protein Sequences journal September 2017
Coniochaeta endophytica sp. nov., a foliar endophyte associated with healthy photosynthetic tissue of Platycladus orientalis (Cupressaceae) journal July 2019
Host and geographic structure of endophytic and endolichenic fungi at a continental scale journal May 2012
Molecular phylogeny of Hypoxylon and closely related genera journal July 2005
Draft genome sequence of the griseofulvin-producing fungus Xylaria flabelliformis strain G536 dataset January 2019
Extensive horizontal gene transfers between plant pathogenic fungi 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 collection January 2018
CAZymes-based ranking of fungi (CBRF): an interactive web database for identifying fungi with extrinsic plant biomass degrading abilities collection January 2019
Ecological generalism drives hyperdiversity of secondary metabolite gene clusters in xylarialean endophytes collection January 2021
Evidence for loss and reacquisition of alcoholic fermentation in a fructophilic yeast lineage journal April 2018
Diversity, taxonomic composition, and functional aspects of fungal communities in living, senesced, and fallen leaves at five sites across North America journal January 2016