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Grant support

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 We thank F. Martin, P. Gladieux, J. Spatafora, R. Vilgalys, and K. O`Donnell for permission to use unpublished JGI F1000 genomes; D. Bellomo, Y. Sanchez-Rosario, and S. Valdez for laboratory assistance; and the Genomics Analysis and Sequencing Core (GATC), the Arizona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.

Analysis of institutional authors

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Article

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

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

Authors: 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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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 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

AlgorithmAscomycotaDatabaseDiversityEndophyteEndophytesEvolutionFamiliesFungiIdentificationLichensMultigene familyPhylogenyPlant-fungal interactionsSaprotrophSoftwareSpecialised metabolismSymbiosisTrophic modeXylariaceaeXylariales

Quality index

Bibliometric impact. Analysis of the contribution and dissemination channel

The work has been published in the journal New Phytologist due to its progression and the good impact it has achieved in recent years, according to the agency WoS (JCR), it has become a reference in its field. In the year of publication of the work, 2022, it was in position 11/239, thus managing to position itself as a Q1 (Primer Cuartil), in the category Plant Sciences. Notably, the journal is positioned above the 90th percentile.

From a relative perspective, and based on the normalized impact indicator calculated from World Citations provided by WoS (ESI, Clarivate), it yields a value for the citation normalization relative to the expected citation rate of: 2.19. This indicates that, compared to works in the same discipline and in the same year of publication, it ranks as a work cited above average. (source consulted: ESI Nov 14, 2024)

This information is reinforced by other indicators of the same type, which, although dynamic over time and dependent on the set of average global citations at the time of their calculation, consistently position the work at some point among the top 50% most cited in its field:

  • Field Citation Ratio (FCR) from Dimensions: 7.15 (source consulted: Dimensions Jun 2025)

Specifically, and according to different indexing agencies, this work has accumulated citations as of 2025-06-07, the following number of citations:

  • WoS: 19
  • Scopus: 26
  • Europe PMC: 15
  • Google Scholar: 34
  • OpenCitations: 27

Impact and social visibility

From the perspective of influence or social adoption, and based on metrics associated with mentions and interactions provided by agencies specializing in calculating the so-called "Alternative or Social Metrics," we can highlight as of 2025-06-07:

  • The use, from an academic perspective evidenced by the Altmetric agency indicator referring to aggregations made by the personal bibliographic manager Mendeley, gives us a total of: 62.
  • The use of this contribution in bookmarks, code forks, additions to favorite lists for recurrent reading, as well as general views, indicates that someone is using the publication as a basis for their current work. This may be a notable indicator of future more formal and academic citations. This claim is supported by the result of the "Capture" indicator, which yields a total of: 61 (PlumX).

With a more dissemination-oriented intent and targeting more general audiences, we can observe other more global scores such as:

  • The Total Score from Altmetric: 30.1.
  • The number of mentions on the social network X (formerly Twitter): 47 (Altmetric).

Leadership analysis of institutional authors

This work has been carried out with international collaboration, specifically with researchers from: Canada; Denmark; France; Saudi Arabia; Taiwan; United Kingdom; United States of America.

There is a significant leadership presence as some of the institution’s authors appear as the first or last signer, detailed as follows: First Author (FRANCO, MARIO EMILIO ERNESTO) .