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

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

New Phytologist, Volume: 233, Issue: 3, Pages: 1317 - 1330

Swansea University Author: Dan Eastwood Orcid Logo

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DOI (Published version): 10.1111/nph.17873

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 metab...

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Published in: New Phytologist
ISSN: 0028-646X 1469-8137
Published: Wiley 2022
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URI: https://cronfa.swan.ac.uk/Record/cronfa59174
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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 substrate 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. 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.
Keywords: Ascomycota; endophyte; plant–fungal interactions; saprotroph; specialised metabolism; symbiosis; trophic mode; Xylariales
College: Faculty of Science and Engineering
Issue: 3
Start Page: 1317
End Page: 1330