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Title: Genomes and secretomes of Ascomycota fungi reveal diverse functions in plant biomass decomposition and pathogenesis

Journal Article · · BMC Genomics

The dominant fungi in arid grasslands and shrublands are members of the Ascomycota phylum. Ascomycota fungi are important drivers in carbon and nitrogen cycling in arid ecosystems. These fungi play roles in soil stability, plant biomass decomposition, and endophytic interactions with plants. They may also form symbiotic associations with biocrust components or be latent saprotrophs or pathogens that live on plant tissues. However, their functional potential in arid soils, where organic matter, nutrients and water are very low or only periodically available, is poorly characterized. Five Ascomycota fungi were isolated from different soil crust microhabitats and rhizosphere soils around the native bunchgrass Pleuraphis jamesii in an arid grassland near Moab, UT, USA. Putative genera were Coniochaeta, isolated from lichen biocrust, Embellisia from cyanobacteria biocrust, Chaetomium from below lichen biocrust, Phoma from a moss microhabitat, and Aspergillus from the soil. The fungi were grown in replicate cultures on different carbon sources (chitin, native bunchgrass or pine wood) relevant to plant biomass and soil carbon sources. Secretomes produced by the fungi on each substrate were characterized. Results demonstrate that these fungi likely interact with primary producers (biocrust or plants) by secreting a wide range of proteins that facilitate symbiotic associations. Each of the fungal isolates secreted enzymes that degrade plant biomass, small secreted effector proteins, and proteins involved in either beneficial plant interactions or virulence. Aspergillus and Phoma expressed more plant biomass degrading enzymes when grown in grass- and pine-containing cultures than in chitin. Coniochaeta and Embellisia expressed similar numbers of these enzymes under all conditions, while Chaetomium secreted more of these enzymes in grass-containing cultures. This study of Ascomycota genomes and secretomes provides important insights about the lifestyles and the roles that Ascomycota fungi likely play in arid grassland, ecosystems. However, the exact nature of those interactions, whether any or all of the isolates are true endophytes, latent saprotrophs or opportunistic phytopathogens, will be the topic of future studies.

Research Organization:
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States). Environmental Molecular Sciences Laboratory (EMSL); Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE National Nuclear Security Administration (NNSA)
Grant/Contract Number:
AC05-76RL01830; 89233218CNA000001
OSTI ID:
1618577
Alternate ID(s):
OSTI ID: 1580512; OSTI ID: 1603981; OSTI ID: 1634951
Report Number(s):
PNNL-SA-140986; LA-UR-16-29573; LA-UR-19-20737; LA-UR-18-25519
Journal Information:
BMC Genomics, Vol. 20, Issue 1; ISSN 1471-2164
Publisher:
SpringerCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 71 works
Citation information provided by
Web of Science

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Relationship Between the Endophyte Embellisia spp. and the Toxic Alkaloid Swainsonine in Major Locoweed Species (Astragalus and Oxytropis) journal December 2007
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The Magnaporthe oryzae Alt A 1-like protein MoHrip1 binds to the plant plasma membrane journal October 2017
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The toxicology mechanism of endophytic fungus and swainsonine in locoweed journal October 2016
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Disruption of the chitin synthase gene CHS1 from Fusarium asiaticum results in an altered structure of cell walls and reduced virulence journal March 2010
Discrete lineages within Alternaria alternata species group: Identification using new highly variable loci and support from morphological characters journal November 2015
Fungi in hot and cold deserts with particular reference to microcolonial fungi journal August 2012
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A general suite of fungal endophytes dominate the roots of two dominant grasses in a semiarid grassland journal January 2010
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Chitin synthesis and fungal pathogenesis journal August 2010
Secreted fungal aspartic proteases: A review journal April 2016
Resolving the Phoma enigma journal September 2015
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Evolution and genome architecture in fungal plant pathogens journal August 2017
Comparative genomics provides insights into the lifestyle and reveals functional heterogeneity of dark septate endophytic fungi journal April 2018
Alternaria spp.: from general saprophyte to specific parasite journal July 2003
Dark septate endophytes: a review of facultative biotrophic root-colonizing fungi journal October 1998
Deciphering the molecular mechanisms behind cellulase production in Trichoderma reesei , the hyper-cellulolytic filamentous fungus journal February 2016
A new species, Embellisia astragali sp. nov., causing standing milk-vetch disease in China journal May 2007
Comparative study of genome-wide plant biomass-degrading CAZymes in white rot, brown rot and soft rot fungi journal December 2017
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Curation of characterized glycoside hydrolases of Fungal origin journal January 2011
Interspecific metabolic diversity of root-colonizing endophytic fungi revealed by enzyme activity tests journal September 2016
Fungal endophytes for sustainable crop production journal September 2016
New insights on trehalose: a multifunctional molecule journal January 2003
AUGUSTUS: ab initio prediction of alternative transcripts journal July 2006
The Pfam protein families database: towards a more sustainable future journal December 2015
Microbe Profile: Aspergillus fumigatus: a saprotrophic and opportunistic fungal pathogen journal August 2018
The Myosin Motor Domain of Fungal Chitin Synthase V Is Dispensable for Vesicle Motility but Required for Virulence of the Maize Pathogen Ustilago maydis journal July 2010
The Nep1-like proteins-a growing family of microbial elicitors of plant necrosis journal July 2004
Host-selective toxins produced by the plant pathogenic fungus Alternaria alternata journal January 2013
Tools of the crook- infection strategies of fungal plant pathogens journal January 2018
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BREAKING AND ENTERING: Host Penetration by the Fungal Rice Blast Pathogen Magnaporthe grisea journal October 1996
Melanin is an essential component for the integrity of the cell wall of Aspergillus fumigatus conidia journal January 2009
Arsenal of plant cell wall degrading enzymes reflects host preference among plant pathogenic fungi journal January 2011
Diverse Lifestyles and Strategies of Plant Pathogenesis Encoded in the Genomes of Eighteen Dothideomycetes Fungi journal December 2012
Swainsonine Biosynthesis Genes in Diverse Symbiotic and Pathogenic Fungi journal April 2017
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Fungal Infection of Plants journal October 1996
DOPA and DHN pathway orchestrate melanin synthesis inAspergillusspecies journal September 2013
A class-wide phylogenetic assessment of Dothideomycetes journal January 2009
Alternaria redefined journal June 2013
Cerato-platanin family proteins: one function for multiple biological roles? journal January 2015
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Plant Bioactive Metabolites and Drugs Produced by Endophytic Fungi of Spermatophyta journal September 2015
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Cellulose Degradation by Oxidative Enzymes journal September 2012