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

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

*Corresponding author for this work

Research output: Contribution to journalJournal articleResearchpeer-review

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Abstract

●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 to more ecologically specialized Hypoxylaceae species. Overall, 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.
Original languageEnglish
JournalNew Phytologist
Volume233
Issue number3
Pages (from-to)1317-1330
Number of pages14
ISSN0028-646X
DOIs
Publication statusPublished - 2022

Keywords

  • Ascomycota
  • Xylariales
  • Endophyte
  • Plant-fungal interactions
  • Saprotroph
  • Specialized metabolism
  • Symbiosis
  • Trophic mode

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