Comparative genomics provides insights into the lifestyle and reveals functional heterogeneity of dark septate endophytic fungi

Knapp, Dániel G.; Németh, Julianna B.; Barry, Kerrie; Hainaut, Matthieu; Henrissat, Bernard; Johnson, Jenifer; Kuo, Alan; Lim, Joanne Hui Ping; Lipzen, Anna; Nolan, Matt; Ohm, Robin A.; Tamás, László; Grigoriev, Igor V.; Spatafora, Joseph W.; Nagy, László G.; Kovács, Gábor M.

doi:10.1038/s41598-018-24686-4

Title: Comparative genomics provides insights into the lifestyle and reveals functional heterogeneity of dark septate endophytic fungi

Journal Article · Fri Apr 20 00:00:00 EDT 2018 · Scientific Reports

DOI:https://doi.org/10.1038/s41598-018-24686-4· OSTI ID:1543779

^[1]; Németh, Julianna B. ^[1]; Barry, Kerrie ^[2]; Hainaut, Matthieu ^[3]; Henrissat, Bernard ^[4]; Johnson, Jenifer ^[2]; Kuo, Alan ^[2]; Lim, Joanne Hui Ping ^[2]; Lipzen, Anna ^[2]; Nolan, Matt ^[2]; Ohm, Robin A. ^[5];

^[1];

^[6]; Spatafora, Joseph W. ^[7];

^[8];

^[9]

Eötvös Loránd Univ., Budapest (Hungary)
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
Aix-Marseille Univ., and CNRS/IN2P3, Marseille (France)
Aix-Marseille Univ., and CNRS/IN2P3, Marseille (France); King Abdulaziz Univ., Jeddah (Saudi Arabia)
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Univ. of Utrecht (Netherlands)
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Univ. of California, Berkeley, CA (United States)
Oregon State Univ., Corvallis, OR (United States)
BRC-HAS, Szeged (Hungary)
Eötvös Loránd Univ., Budapest (Hungary); Hungarian Academy of Sciences, Budapest (Hungary)

Dark septate endophytes (DSE) are a form-group of root endophytic fungi with elusive functions. Here, the genomes of two common DSE of semiarid areas, Cadophora sp. and Periconia macrospinosa were sequenced and analyzed with another 32 ascomycetes of different lifestyles. Cadophora sp. (Helotiales) and P. macrospinosa (Pleosporales) have genomes of 70.46 Mb and 54.99 Mb with 22,766 and 18,750 gene models, respectively. The majority of DSE-specific protein clusters lack functional annotation with no similarity to characterized proteins, implying that they have evolved unique genetic innovations. Both DSE possess an expanded number of carbohydrate active enzymes (CAZymes), including plant cell wall degrading enzymes (PCWDEs). Those were similar in three other DSE, and contributed a signal for the separation of root endophytes in principal component analyses of CAZymes, indicating shared genomic traits of DSE fungi. Number of secreted proteases and lipases, aquaporins, and genes linked to melanin synthesis were also relatively high in our fungi. In spite of certain similarities between our two DSE, we observed low levels of convergence in their gene family evolution. This suggests that, despite originating from the same habitat, these two fungi evolved along different evolutionary trajectories and display considerable functional differences within the endophytic lifestyle.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC); Univ. of California, Oakland, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC); Hungarian Scientific Research Fund

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1543779

Alternate ID(s):: OSTI ID: 1619098

Journal Information:: Scientific Reports, Vol. 8, Issue 1; ISSN 2045-2322

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 98 works

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Differential interaction of the dark septate endophyte Cadophora sp. and fungal pathogens in vitro and in planta Yakti, Wael; Kovács, Gábor M.; Franken, Philipp FEMS Microbiology Ecology, Vol. 95, Issue 12 https://doi.org/10.1093/femsec/fiz164	journal	October 2019
Novel phylogenetic methods are needed for understanding gene function in the era of mega-scale genome sequencing Nagy, László G.; Merényi, Zsolt; Hegedüs, Botond Nucleic Acids Research, Vol. 48, Issue 5 https://doi.org/10.1093/nar/gkz1241	journal	January 2020
Comparative genomics applied to Mucor species with different lifestyles Lebreton, Annie; Corre, Erwan; Jany, Jean-Luc BMC Genomics, Vol. 21, Issue 1 https://doi.org/10.1186/s12864-019-6256-2	journal	February 2020
Genomes and secretomes of Ascomycota fungi reveal diverse functions in plant biomass decomposition and pathogenesis Challacombe, Jean F.; Hesse, Cedar N.; Bramer, Lisa M. BMC Genomics, Vol. 20, Issue 1 https://doi.org/10.1186/s12864-019-6358-x	journal	December 2019
Genome-scale data resolve ancestral rock-inhabiting lifestyle in Dothideomycetes (Ascomycota) Ametrano, Claudio G.; Grewe, Felix; Crous, Pedro W. IMA Fungus, Vol. 10, Issue 1 https://doi.org/10.1186/s43008-019-0018-2	journal	October 2019
Extensive sampling and high-throughput sequencing reveal Posidoniomyces atricolor gen. et sp. nov. (Aigialaceae, Pleosporales) as the dominant root mycobiont of the dominant Mediterranean seagrass Posidonia oceanica Vohník, Martin; Borovec, Ondřej; Kolaříková, Zuzana MycoKeys, Vol. 55 https://doi.org/10.3897/mycokeys.55.35682	journal	June 2019
Hemiparasitic plants increase alpine plant richness and evenness but reduce arbuscular mycorrhizal fungal colonization in dominant plant species McKibben, Michael; Henning, Jeremiah A. PeerJ, Vol. 6 https://doi.org/10.7717/peerj.5682	journal	January 2018
Hiding in plain sight: New virus genomes discovered via a systematic analysis of fungal public transcriptomes Gilbert, Kerrigan B.; Holcomb, Emily E.; Allscheid, Robyn L. PLOS ONE, Vol. 14, Issue 7 https://doi.org/10.1371/journal.pone.0219207	journal	July 2019
Root-Colonizing Endophytic Fungi of the Dominant Grass Stipa krylovii From a Mongolian Steppe Grassland Knapp, Dániel G.; Imrefi, Ildikó; Boldpurev, Enkhtuul Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.02565	journal	November 2019
Rapid Divergence of Genome Architectures Following the Origin of an Ectomycorrhizal Symbiosis in the Genus Amanita Hess, Jaqueline; Skrede, Inger; Chaib De Mares, Maryam Molecular Biology and Evolution https://doi.org/10.1093/molbev/msy179	journal	September 2018

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