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

Abstract

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.

Authors:
ORCiD logo [1];  [1];  [2];  [3];  [4];  [2];  [2];  [2];  [2];  [2];  [5]; ORCiD logo [1]; ORCiD logo [6];  [7]; ORCiD logo [8]; ORCiD logo [9]
  1. Eötvös Loránd Univ., Budapest (Hungary)
  2. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  3. Aix-Marseille Univ., and CNRS/IN2P3, Marseille (France)
  4. Aix-Marseille Univ., and CNRS/IN2P3, Marseille (France); King Abdulaziz Univ., Jeddah (Saudi Arabia)
  5. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Univ. of Utrecht (Netherlands)
  6. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Univ. of California, Berkeley, CA (United States)
  7. Oregon State Univ., Corvallis, OR (United States)
  8. BRC-HAS, Szeged (Hungary)
  9. Eötvös Loránd Univ., Budapest (Hungary); Hungarian Academy of Sciences, Budapest (Hungary)
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC); Univ. of California, Oakland, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC); Hungarian Scientific Research Fund
OSTI Identifier:
1543779
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Scientific Reports
Additional Journal Information:
Journal Volume: 8; Journal Issue: 1; Journal ID: ISSN 2045-2322
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

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., and Kovács, Gábor M. Comparative genomics provides insights into the lifestyle and reveals functional heterogeneity of dark septate endophytic fungi. United States: N. p., 2018. Web. doi:10.1038/s41598-018-24686-4.
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. Comparative genomics provides insights into the lifestyle and reveals functional heterogeneity of dark septate endophytic fungi. United States. doi:10.1038/s41598-018-24686-4.
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., and Kovács, Gábor M. Fri . "Comparative genomics provides insights into the lifestyle and reveals functional heterogeneity of dark septate endophytic fungi". United States. doi:10.1038/s41598-018-24686-4. https://www.osti.gov/servlets/purl/1543779.
@article{osti_1543779,
title = {Comparative genomics provides insights into the lifestyle and reveals functional heterogeneity of dark septate endophytic fungi},
author = {Knapp, Dániel G. and Németh, Julianna B. and Barry, Kerrie and Hainaut, Matthieu and Henrissat, Bernard and Johnson, Jenifer and Kuo, Alan and Lim, Joanne Hui Ping and Lipzen, Anna and Nolan, Matt and Ohm, Robin A. and Tamás, László and Grigoriev, Igor V. and Spatafora, Joseph W. and Nagy, László G. and Kovács, Gábor M.},
abstractNote = {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.},
doi = {10.1038/s41598-018-24686-4},
journal = {Scientific Reports},
number = 1,
volume = 8,
place = {United States},
year = {2018},
month = {4}
}

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