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Title: Diverse plant-associated pleosporalean fungi from saline areas: Ecological tolerance and nitrogen-status dependent effects on plant growth

Abstract

Similar to mycorrhizal mutualists, the rhizospheric and endophytic fungi are also considered to act as active regulators of host fitness (e.g., nutrition and stress tolerance). Despite considerable work in selected model systems, it is generally poorly understood how plant-associated fungi are structured in habitats with extreme conditions and to what extent they contribute to improved plant performance. Here, we investigate the community composition of root and seed-associated fungi from six halophytes growing in saline areas of China, and found that the pleosporalean taxa (Ascomycota) were most frequently isolated across samples. A total of twenty-seven representative isolates were selected for construction of the phylogeny based on the multi-locus data (partial 18S rDNA, 28S rDNA, and transcription elongation factor 1-a), which classified them into seven families, one clade potentially representing a novel lineage. Fungal isolates were subjected to growth response assays by imposing temperature, pH, ionic and osmotic conditions. The fungi had a wide pH tolerance, while most isolates showed a variable degree of sensitivity to increasing concentration of either salt or sorbitol. Subsequent plant fungal co-culture assays indicated that most isolates had only neutral or even adverse effects on plant growth in the presence of inorganic nitrogen. Interestingly, when provided withmore » organic nitrogen sources the majority of the isolates enhanced plant growth especially above ground biomass. Most of the fungi preferred organic nitrogen over its inorganic counterpart, suggesting that these fungi can readily mineralize organic nitrogen into inorganic nitrogen. Microscopy revealed that several isolates can successfully colonize roots and form melanized hyphae and/or microsclerotia-like structures within cortical cells suggesting a phylogenetic assignment as dark septate endophytes. Furthermore, this work provides a better understanding of the symbiotic relationship between plants and pleosporalean fungi, and initial evidence for the use of this fungal group in benefiting plant production.« less

Authors:
 [1];  [1];  [2];  [2];  [2];  [3];  [1]
  1. Chinese Academy of Forestry, Hangzhou (China)
  2. TU Wien, Vienna (Austria)
  3. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Publication Date:
Research Org.:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1342709
Grant/Contract Number:  
AC05-00OR22725
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Volume: 8; Journal Issue: 8; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES; Fungi; Nitrogen; Ecological Tolearance; Saline Tolerance

Citation Formats

Qin, Yuan, Pan, Xueyu, Kubicek, Christian, Druzhinina, Irina, Chenthamara, Komal, Labbe, Jessy, and Yuan, Zhilin. Diverse plant-associated pleosporalean fungi from saline areas: Ecological tolerance and nitrogen-status dependent effects on plant growth. United States: N. p., 2017. Web. doi:10.3389/fmicb.2017.00158.
Qin, Yuan, Pan, Xueyu, Kubicek, Christian, Druzhinina, Irina, Chenthamara, Komal, Labbe, Jessy, & Yuan, Zhilin. Diverse plant-associated pleosporalean fungi from saline areas: Ecological tolerance and nitrogen-status dependent effects on plant growth. United States. https://doi.org/10.3389/fmicb.2017.00158
Qin, Yuan, Pan, Xueyu, Kubicek, Christian, Druzhinina, Irina, Chenthamara, Komal, Labbe, Jessy, and Yuan, Zhilin. Mon . "Diverse plant-associated pleosporalean fungi from saline areas: Ecological tolerance and nitrogen-status dependent effects on plant growth". United States. https://doi.org/10.3389/fmicb.2017.00158. https://www.osti.gov/servlets/purl/1342709.
@article{osti_1342709,
title = {Diverse plant-associated pleosporalean fungi from saline areas: Ecological tolerance and nitrogen-status dependent effects on plant growth},
author = {Qin, Yuan and Pan, Xueyu and Kubicek, Christian and Druzhinina, Irina and Chenthamara, Komal and Labbe, Jessy and Yuan, Zhilin},
abstractNote = {Similar to mycorrhizal mutualists, the rhizospheric and endophytic fungi are also considered to act as active regulators of host fitness (e.g., nutrition and stress tolerance). Despite considerable work in selected model systems, it is generally poorly understood how plant-associated fungi are structured in habitats with extreme conditions and to what extent they contribute to improved plant performance. Here, we investigate the community composition of root and seed-associated fungi from six halophytes growing in saline areas of China, and found that the pleosporalean taxa (Ascomycota) were most frequently isolated across samples. A total of twenty-seven representative isolates were selected for construction of the phylogeny based on the multi-locus data (partial 18S rDNA, 28S rDNA, and transcription elongation factor 1-a), which classified them into seven families, one clade potentially representing a novel lineage. Fungal isolates were subjected to growth response assays by imposing temperature, pH, ionic and osmotic conditions. The fungi had a wide pH tolerance, while most isolates showed a variable degree of sensitivity to increasing concentration of either salt or sorbitol. Subsequent plant fungal co-culture assays indicated that most isolates had only neutral or even adverse effects on plant growth in the presence of inorganic nitrogen. Interestingly, when provided with organic nitrogen sources the majority of the isolates enhanced plant growth especially above ground biomass. Most of the fungi preferred organic nitrogen over its inorganic counterpart, suggesting that these fungi can readily mineralize organic nitrogen into inorganic nitrogen. Microscopy revealed that several isolates can successfully colonize roots and form melanized hyphae and/or microsclerotia-like structures within cortical cells suggesting a phylogenetic assignment as dark septate endophytes. Furthermore, this work provides a better understanding of the symbiotic relationship between plants and pleosporalean fungi, and initial evidence for the use of this fungal group in benefiting plant production.},
doi = {10.3389/fmicb.2017.00158},
journal = {Frontiers in Microbiology},
number = 8,
volume = 8,
place = {United States},
year = {Mon Feb 06 00:00:00 EST 2017},
month = {Mon Feb 06 00:00:00 EST 2017}
}

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Dark septate root endophytic fungi increase growth of Scots pine seedlings under elevated CO2 through enhanced nitrogen use efficiency
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Effect of NaCl reduction and replacement on the growth of fungi important to the spoilage of bread
journal, September 2010


Assimilation of organic and inorganic nutrients by Erica root fungi from the fynbos ecosystem
journal, March 2016


Mycorrhizas and dark septate root endophytes in polar regions
journal, February 2009


A fine line – endophytes or pathogens in Arabidopsis thaliana
journal, December 2012


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


Broad compatibility in fungal root symbioses
journal, August 2014


Alternaria section Alternaria: Species, formae speciales or pathotypes?
journal, September 2015


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


Major lineages of Dothideomycetes (Ascomycota) inferred from SSU and LSU rDNA sequences
journal, August 2001


Stress tolerance in plants via habitat-adapted symbiosis
journal, February 2008

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  • DOI: 10.1038/ismej.2007.106

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Trichoderma: the genomics of opportunistic success
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  • Nature Reviews Microbiology, Vol. 9, Issue 10
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MRBAYES: Bayesian inference of phylogenetic trees
journal, August 2001


AliView: a fast and lightweight alignment viewer and editor for large datasets
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Interspecific metabolic diversity of root-colonizing endophytic fungi revealed by enzyme activity tests
journal, September 2016

  • Knapp, Dániel G.; Kovács, Gábor M.
  • FEMS Microbiology Ecology, Vol. 92, Issue 12
  • DOI: 10.1093/femsec/fiw190

Characterization of rhizosphere fungi that mediate resistance in tomato against bacterial wilt disease
journal, August 2013

  • Jogaiah, Sudisha; Abdelrahman, Mostafa; Tran, Lam-Son Phan
  • Journal of Experimental Botany, Vol. 64, Issue 12
  • DOI: 10.1093/jxb/ert212

MUSCLE: multiple sequence alignment with high accuracy and high throughput
journal, March 2004

  • Edgar, R. C.
  • Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797
  • DOI: 10.1093/nar/gkh340

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A Rhizosphere Fungus Enhances Arabidopsis Thermotolerance through Production of an HSP90 Inhibitor
journal, July 2007

  • McLellan, Catherine A.; Turbyville, Thomas J.; Wijeratne, E. M. Kithsiri
  • Plant Physiology, Vol. 145, Issue 1
  • DOI: 10.1104/pp.107.101808

Trichoderma virens , a Plant Beneficial Fungus, Enhances Biomass Production and Promotes Lateral Root Growth through an Auxin-Dependent Mechanism in Arabidopsis
journal, January 2009

  • Contreras-Cornejo, Hexon Angel; Macías-Rodríguez, Lourdes; Cortés-Penagos, Carlos
  • Plant Physiology, Vol. 149, Issue 3
  • DOI: 10.1104/pp.108.130369

Piriformospora indica affects plant growth by auxin production
journal, December 2007


Mycorrhizal diversity in arctic and alpine tundra: an open question
journal, May 1996


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


Endophytic Insect-Parasitic Fungi Translocate Nitrogen Directly from Insects to Plants
journal, June 2012


Extensive Fungal Diversity in Plant Roots
journal, March 2002


Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species.
journal, August 1990


Alkaliphiles: Some Applications of Their Products for Biotechnology
journal, December 1999


Induced Systemic Resistance and Plant Responses to Fungal Biocontrol Agents
journal, July 2010


Muriphaeosphaeria galatellae gen. et sp. nov. in Phaeosphaeriaceae (Pleosporales)
journal, September 2015

  • Phukhamsakda, Chayanard; Ariyawansa, Hiran A.; Phookamsak, Rungtiwa
  • Phytotaxa, Vol. 227, Issue 1
  • DOI: 10.11646/phytotaxa.227.1.6

Phylogeny and morphology of Premilcurensis gen. nov. (Pleosporales) from stems of Senecio in Italy
journal, November 2015

  • Tibpromma, Saowaluck; Promputtha, Itthayakorn; Phookamsak, Rungtiwa
  • Phytotaxa, Vol. 236, Issue 1
  • DOI: 10.11646/phytotaxa.236.1.3

Phylogenetic diversity of stress signaling pathways in fungi
journal, January 2009

  • Nikolaou, Elissavet; Agriafioti, Ino; Stumpf, Michael
  • BMC Evolutionary Biology, Vol. 9, Issue 1
  • DOI: 10.1186/1471-2148-9-44

Increased Fitness of Rice Plants to Abiotic Stress Via Habitat Adapted Symbiosis: A Strategy for Mitigating Impacts of Climate Change
journal, July 2011


Endophyte Microbiome Diversity in Micropropagated Atriplex canescens and Atriplex torreyi var griffithsii
journal, March 2011


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


A New Fungal Endophyte, Scolecobasidium humicola, Promotes Tomato Growth under Organic Nitrogen Conditions
journal, November 2013


Evidences on the Ability of Mycorrhizal Genus Piloderma to Use Organic Nitrogen and Deliver It to Scots Pine
journal, July 2015


In Vitro Morphogenesis of Arabidopsis to Search for Novel Endophytic Fungi Modulating Plant Growth
journal, December 2015


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

  • Caldwell, Bruce A.; Jumpponen, Ari; Trappe, James M.
  • Mycologia, Vol. 92, Issue 2
  • DOI: 10.2307/3761555

Multi-locus phylogeny of Pleosporales: a taxonomic, ecological and evolutionary re-evaluation
journal, January 2009


Molecular taxonomy of bambusicolous fungi: Tetraplosphaeriaceae, a new pleosporalean family with Tetraploa-like anamorphs
journal, January 2009


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


Alternaria redefined
journal, June 2013

  • Woudenberg, J. H. C.; Groenewald, J. Z.; Binder, M.
  • Studies in Mycology, Vol. 75
  • DOI: 10.3114/sim0015

Sizing up Septoria
journal, June 2013

  • Quaedvlieg, W.; Verkley, G. J. M.; Shin, H. -D.
  • Studies in Mycology, Vol. 75
  • DOI: 10.3114/sim0017

Novel genera and species of coniothyrium-like fungi in Montagnulaceae ( Ascomycota )
journal, June 2014

  • Verkley, G. J. M.; Dukik, K.; Renfurm, R.
  • Persoonia - Molecular Phylogeny and Evolution of Fungi, Vol. 32, Issue 1
  • DOI: 10.3767/003158514x679191

A molecular phylogenetic assessment of Massarina ingoldiana sensu lato
journal, May 2010

  • Hirayama, Kazuyuki; Tanaka, Kazuaki; Raja, Huzefa A.
  • Mycologia, Vol. 102, Issue 3
  • DOI: 10.3852/09-230

Systematic reappraisal of species in Phoma section Paraphoma , Pyrenochaeta and Pleurophoma
journal, September 2010

  • de Gruyter, Johannes; Woudenberg, Joyce H. C.; Aveskamp, Maikel M.
  • Mycologia, Vol. 102, Issue 5
  • DOI: 10.3852/09-240

A multigene phylogeny of the Dothideomycetes using four nuclear loci
journal, November 2006


Nutrient transfer to plants by phylogenetically diverse fungi suggests convergent evolutionary strategies in rhizospheric symbionts
journal, January 2013

  • Behie, Scott W.; Padilla-Guerrero, Israel E.; Bidochka, Michael J.
  • Communicative & Integrative Biology, Vol. 6, Issue 1
  • DOI: 10.4161/cib.22321

Unraveling the role of fungal symbionts in plant abiotic stress tolerance
journal, February 2011

  • Singh, Lamabam Peter; Gill, Sarvajeet Singh; Tuteja, Narendra
  • Plant Signaling & Behavior, Vol. 6, Issue 2
  • DOI: 10.4161/psb.6.2.14146

Works referencing / citing this record:

Identification, ecological evaluation and phylogenetic analysis of non-symbiotic endophytic fungi colonizing timothy grass and perennial ryegrass grown in adjacent plots
journal, January 2019

  • Przemieniecki, Sebastian Wojciech; Damszel, Marta; Kurowski, Tomasz Paweł
  • Grass and Forage Science, Vol. 74, Issue 1
  • DOI: 10.1111/gfs.12404

Effects of endophytic and ectomycorrhizal basidiomycetes on Quercus virginiana seedling growth and nutrient absorption
journal, January 2019


Funneliformis mosseae Enhances Root Development and Pb Phytostabilization in Robinia pseudoacacia in Pb-Contaminated Soil
journal, November 2019


Dark Septate Endophytic Fungi Help Tomato to Acquire Nutrients from Ground Plant Material
journal, December 2017

  • Vergara, Carlos; Araujo, Karla E. C.; Urquiaga, Segundo
  • Frontiers in Microbiology, Vol. 8
  • DOI: 10.3389/fmicb.2017.02437

Funneliformis mosseae Enhances Root Development and Pb Phytostabilization in Robinia pseudoacacia in Pb-Contaminated Soil
journal, November 2019


Dark Septate Endophytic Fungi Increase Green Manure-15N Recovery Efficiency, N Contents, and Micronutrients in Rice Grains
journal, May 2018

  • Vergara, Carlos; Araujo, Karla E. C.; Urquiaga, Segundo
  • Frontiers in Plant Science, Vol. 9
  • DOI: 10.3389/fpls.2018.00613