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Funding for the project was provided by the DOE JGI Large-scale Community Science Project (Grant no. 503506 to JMU, JHW, AEA). MEEF was funded by the Office for Research, Innovation and Impact at the University of Arizona and the University of Arizona BIO5 Postdoctoral Fellowship Program. FL and JM received financial support from NSF DEB-1541548 and DEB-1046065, and AEA received support from NSF DEB-1541496 and DEB-1045766. These awards and NSF DEB-0640996 to AEA and DEB-1010675 to AEA and JMU supported the initial collections of endophytes. We thank F. Martin, P. Gladieux, J. Spatafora, R. Vilgalys, and K. O`Donnell for permission to use unpublished JGI F1000 genomes; D. Bellomo, Y. Sanchez-Rosario, and S. Valdez for laboratory assistance; and the Genomics Analysis and Sequencing Core (GATC), the Arizona Genomics Institute (AGI), and the High-Performance Computer (HPC) at the University of Arizona for technical support. The authors declare no competing interests.

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

Publicado en:New Phytologist. 233 (3): 1317-1330 - 2022-02-01 233(3), DOI: 10.1111/nph.17873

Autores: 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, Francois; Miadlikowska, Jolanta; Eastwood, Daniel C; Hamelin, Richard C; Grigoriev, Igor, V; U'Ren, Jana M

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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. 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.

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