skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

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 Lab. (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
Alternate Identifier(s):
OSTI ID: 1619098
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Journal Article: 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. https://doi.org/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. https://doi.org/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},
url = {https://www.osti.gov/biblio/1543779}, journal = {Scientific Reports},
issn = {2045-2322},
number = 1,
volume = 8,
place = {United States},
year = {2018},
month = {4}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 25 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Extensive Fungal Diversity in Plant Roots
journal, March 2002


raxmlGUI: a graphical front-end for RAxML
journal, September 2011


A meta-analysis of plant responses to dark septate root endophytes
journal, January 2011


Diversity and distribution of soil fungal communities in a semiarid grassland
journal, January 2011


Utilization of Major Detrital Substrates by Dark-Septate, Root Endophytes
journal, March 2000


An Antarctic Hot Spot for Fungi at Shackleton's Historic Hut on Cape Royds
journal, April 2010


Genome evolution in filamentous plant pathogens: why bigger can be better
journal, May 2012


The genome of Xylona heveae provides a window into fungal endophytism
journal, January 2016


Fungal endophytes: diversity and functional roles
journal, February 2009


Fungal diversity in soils and historic wood from the Ross Sea Region of Antarctica
journal, October 2006


Exploring the genomic diversity of black yeasts and relatives ( Chaetothyriales , Ascomycota )
journal, March 2017


Draft Genome Sequence of Microdochium bolleyi , a Dark Septate Fungal Endophyte of Beach Grass
journal, April 2016


High-quality draft assemblies of mammalian genomes from massively parallel sequence data
journal, December 2010


SignalP 4.0: discriminating signal peptides from transmembrane regions
journal, September 2011


A Secreted Effector Protein of Laccaria bicolor Is Required for Symbiosis Development
journal, July 2011


The impact of transposable elements in environmental adaptation
journal, January 2013


The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics
journal, January 2009


Twenty years of the MEROPS database of proteolytic enzymes, their substrates and inhibitors
journal, November 2015


The Plant Cell Wall-Decomposing Machinery Underlies the Functional Diversity of Forest Fungi
journal, July 2011


The endophytic continuum
journal, June 2005


Plant-Symbiotic Fungi as Chemical Engineers: Multi-Genome Analysis of the Clavicipitaceae Reveals Dynamics of Alkaloid Loci
journal, February 2013


Seeking the elusive function of the root-colonising dark septate endophytic fungi
journal, January 2005


Survival trade-offs in plant roots during colonization by closely related beneficial and pathogenic fungi
journal, May 2016


Genome sequencing provides insight into the reproductive biology, nutritional mode and ploidy of the fern pathogen Mixia osmundae
journal, December 2013


The carbohydrate-active enzymes database (CAZy) in 2013
journal, November 2013


Dissecting endophytic lifestyle along the parasitism/mutualism continuum in Arabidopsis
journal, August 2016


Local Modulation of Host pH by Colletotrichum Species as a Mechanism to Increase Virulence
journal, September 2001


Dark septate endophytes: a review of facultative biotrophic root-colonizing fungi
journal, October 1998


An efficient algorithm for large-scale detection of protein families
journal, April 2002


Comparative genome sequence analysis underscores mycoparasitism as the ancestral life style of Trichoderma
journal, April 2011


Novel Root Fungal Consortium Associated with a Dominant Desert Grass
journal, March 2008


Rnnotator: an automated de novo transcriptome assembly pipeline from stranded RNA-Seq reads
journal, January 2010


MycoCosm portal: gearing up for 1000 fungal genomes
journal, December 2013


A secreted lipase of Fusarium graminearum is a virulence factor required for infection of cereals: Lipase as a virulence factor
journal, February 2005


Comparative genomic and transcriptomic analyses reveal the hemibiotrophic stage shift of Colletotrichum fungi
journal, December 2012


Extensive sampling of basidiomycete genomes demonstrates inadequacy of the white-rot/brown-rot paradigm for wood decay fungi
journal, June 2014


The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis
journal, March 2008


FUNGAL ENDOPHYTES: A Continuum of Interactions with Host Plants
journal, November 1998


TreeFix: Statistically Informed Gene Tree Error Correction Using Species Trees
journal, November 2012


Transcriptional regulation of meiosis in yeast
journal, June 2000


The Hidden World within Plants: Ecological and Evolutionary Considerations for Defining Functioning of Microbial Endophytes
journal, July 2015


Genome Expansion and Gene Loss in Powdery Mildew Fungi Reveal Tradeoffs in Extreme Parasitism
journal, December 2010


Hidden Fungi, Emergent Properties: Endophytes and Microbiomes
journal, September 2011


Revision of the Massarineae (Pleosporales, Dothideomycetes)
journal, September 2015


Fungal Effectors and Plant Susceptibility
journal, April 2015


A Neural Network Method for Identification of Prokaryotic and Eukaryotic Signal Peptides and Prediction of their Cleavage Sites
journal, October 1997


Périgord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis
journal, March 2010


The diversity of fungal genome
journal, April 2015


Ectomycorrhizal ecology is imprinted in the genome of the dominant symbiotic fungus Cenococcum geophilum
journal, September 2016


Conserved Meiotic Machinery in Glomus spp., a Putatively Ancient Asexual Fungal Lineage
journal, January 2011


The importance of the microbiome of the plant holobiont
journal, February 2015


Velvet: Algorithms for de novo short read assembly using de Bruijn graphs
journal, February 2008


Interspecific metabolic diversity of root-colonizing endophytic fungi revealed by enzyme activity tests
journal, September 2016


Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans
journal, September 2009


A general suite of fungal endophytes dominate the roots of two dominant grasses in a semiarid grassland
journal, January 2010


Lifestyle transitions in plant pathogenic Colletotrichum fungi deciphered by genome and transcriptome analyses
journal, August 2012


Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists
journal, February 2015


Draft Genome Sequence of Colletotrichum acutatum Sensu Lato (Colletotrichum fioriniae)
journal, March 2014


Metarhizium anisopliae lipolytic activity plays a pivotal role in Rhipicephalus (Boophilus) microplus infection
journal, January 2010


Dark septate endophytic pleosporalean genera from semiarid areas
journal, December 2015


Latent homology and convergent regulatory evolution underlies the repeated emergence of yeasts
journal, July 2014


The Dark Side Is Not Fastidious – Dark Septate Endophytic Fungi of Native and Invasive Plants of Semiarid Sandy Areas
journal, February 2012


Associations between microfungal endophytes and roots: do structural features indicate function?
journal, May 2008


New subfamilies of major intrinsic proteins in fungi suggest novel transport properties in fungal channels: implications for the host-fungal interactions
journal, August 2014


Microfungal endophytes in roots
journal, January 2005


Diverse Lifestyles and Strategies of Plant Pathogenesis Encoded in the Genomes of Eighteen Dothideomycetes Fungi
journal, December 2012


Septate endophyte colonization and host responses of grasses and forbs native to a tallgrass prairie
journal, May 2011


Synthesis and assembly of fungal melanin
journal, December 2011


Biosynthesis of fungal melanins and their importance for human pathogenic fungi
journal, March 2003


The effects of fungal root endophytes on plant growth: a meta-analysis
journal, July 2012


The rice endophyte Harpophora oryzae genome reveals evolution from a pathogen to a mutualistic endophyte
journal, July 2014


Saccharomyces Genome Database: the genomics resource of budding yeast
journal, November 2011


MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0
journal, October 2013


Globally distributed root endophyte Phialocephala subalpina links pathogenic and saprophytic lifestyles
journal, December 2016


Unearthing the roots of ectomycorrhizal symbioses
journal, October 2016


Expansion of the enzymatic repertoire of the CAZy database to integrate auxiliary redox enzymes
journal, January 2013


A Developmentally Regulated Gene Cluster Involved in Conidial Pigment Biosynthesis in Aspergillus fumigatus
journal, October 1999


The Developmentally Regulated alb1 Gene ofAspergillus fumigatus: Its Role in Modulation of Conidial Morphology and Virulence
journal, June 1998


    Works referencing / citing this record:

    Genome-scale data resolve ancestral rock-inhabiting lifestyle in Dothideomycetes (Ascomycota)
    journal, October 2019


    Root-Colonizing Endophytic Fungi of the Dominant Grass Stipa krylovii From a Mongolian Steppe Grassland
    journal, November 2019


    Differential interaction of the dark septate endophyte Cadophora sp. and fungal pathogens in vitro and in planta
    journal, October 2019


    Impact of dark septate endophytes on tomato growth and nutrient uptake
    journal, November 2018


    Genomes and secretomes of Ascomycota fungi reveal diverse functions in plant biomass decomposition and pathogenesis
    journal, December 2019


    Comparative genomics applied to Mucor species with different lifestyles
    journal, February 2020


    Novel phylogenetic methods are needed for understanding gene function in the era of mega-scale genome sequencing
    journal, January 2020