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Title: Comparative genomics and transcriptomics depict ericoid mycorrhizal fungi as versatile saprotrophs and plant mutualists

Abstract

Some soil fungi in the Leotiomycetes form ericoid mycorrhizal (ERM) symbioses with Ericaceae. In the harsh habitats in which they occur, ERM plant survival relies on nutrient mobilization from soil organic matter (SOM) by their fungal partners. The characterization of the fungal genetic machinery underpinning both the symbiotic lifestyle and SOM degradation is needed to understand ERM symbiosis functioning and evolution, and its impact on soil carbon (C) turnover. We sequenced the genomes of the ERM fungi Meliniomyces bicolor, M. variabilis, Oidiodendron maius and Rhizoscyphus ericae, and compared their gene repertoires with those of fungi with different lifestyles (ecto- and orchid mycorrhiza, endophytes, saprotrophs, pathogens). We also identified fungal transcripts induced in symbiosis. The ERM fungal gene contents for polysaccharide-degrading enzymes, lipases, proteases and enzymes involved in secondary metabolism are closer to those of saprotrophs and pathogens than to those of ectomycorrhizal symbionts. The fungal genes most highly upregulated in symbiosis are those coding for fungal and plant cell wall-degrading enzymes (CWDEs), lipases, proteases, transporters and mycorrhiza-induced small secreted proteins (MiSSPs). The ERM fungal gene repertoire reveals a capacity for a dual saprotrophic and biotrophic lifestyle. This may reflect an incomplete transition from saprotrophy to the mycorrhizal habit, or a versatilemore » life strategy similar to fungal endophytes.« less

Authors:
ORCiD logo [1];  [2];  [3];  [4];  [2];  [5];  [4];  [2];  [4];  [4];  [6];  [4];  [4];  [7];  [4];  [4];  [5];  [8];  [2];  [9] more »;  [10];  [11];  [4];  [12];  [13];  [4]; ORCiD logo [2];  [5] « less
  1. Department of Life Sciences and Systems Biology; University of Turin; Turin 10125 Italy;INRA; UMR 1136 INRA-Université de Lorraine ‘Interactions Arbres/Microorganismes’; Laboratoire d'Excellence ARBRE; Centre INRA-Lorraine; 54280 Champenoux France
  2. INRA; UMR 1136 INRA-Université de Lorraine ‘Interactions Arbres/Microorganismes’; Laboratoire d'Excellence ARBRE; Centre INRA-Lorraine; 54280 Champenoux France
  3. Manaaki Whenua - Landcare Research, Ecosystems and Global Change Team; Gerald Street PO Box 69040 Lincoln 7640 New Zealand
  4. US Department of Energy Joint Genome Institute; Walnut Creek CA 94598 USA
  5. Department of Life Sciences and Systems Biology; University of Turin; Turin 10125 Italy
  6. Architecture et Fonction des Macromolécules Biologiques; UMR7257 Centre National de la Recherche Scientifique - Aix-Marseille Université; Case 932, 163 Avenue de Luminy Marseille 13288 France;INRA; USC 1408 AFMB; Marseille 13288 France
  7. Department of Soil and Environment; Swedish University of Agricultural Sciences; Uppsala 75007 Sweden
  8. Pacific Northwest National Laboratory; Chemical and Biological Process Development Group; Richland WA 99354 USA
  9. US Department of Energy Joint Genome Institute; Walnut Creek CA 94598 USA;Microbiology, Department of Biology; Utrecht University; 3508 TB Utrecht the Netherlands
  10. Biological Systems and Engineering Division; Lawrence Berkeley National Laboratory; Berkeley CA 94720 USA
  11. Department of Botany and Plant Pathology; Oregon State University; Corvallis OR 97331 USA
  12. INRA; UMR 1136 INRA-Université de Lorraine ‘Interactions Arbres/Microorganismes’; Laboratoire d'Excellence ARBRE; Centre INRA-Lorraine; 54280 Champenoux France;Laboratoire d'Excellence ARBRE; Faculté des Sciences et Technologies; UMR 1136 INRA-Université de Lorraine ‘Interactions Arbres/Microorganismes’; Université de Lorraine; Campus Aiguillettes, BP 70239 Vandoeuvre les Nancy cedex 54506 France
  13. Architecture et Fonction des Macromolécules Biologiques; UMR7257 Centre National de la Recherche Scientifique - Aix-Marseille Université; Case 932, 163 Avenue de Luminy Marseille 13288 France;INRA; USC 1408 AFMB; Marseille 13288 France;Department of Biological Sciences; King Abdulaziz University - KSA; Jeddah 21589 Saudi Arabia
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)
OSTI Identifier:
1619093
DOE Contract Number:  
AC02-05CH11231
Resource Type:
Journal Article
Journal Name:
New Phytologist
Additional Journal Information:
Journal Volume: 217; Journal Issue: 3; Journal ID: ISSN 0028-646X
Publisher:
Wiley
Country of Publication:
United States
Language:
English

Citation Formats

Martino, Elena, Morin, Emmanuelle, Grelet, Gwen-Aëlle, Kuo, Alan, Kohler, Annegret, Daghino, Stefania, Barry, Kerrie W., Cichocki, Nicolas, Clum, Alicia, Dockter, Rhyan B., Hainaut, Matthieu, Kuo, Rita C., LaButti, Kurt, Lindahl, Björn D., Lindquist, Erika A., Lipzen, Anna, Khouja, Hassine-Radhouane, Magnuson, Jon, Murat, Claude, Ohm, Robin A., Singer, Steven W., Spatafora, Joseph W., Wang, Mei, Veneault-Fourrey, Claire, Henrissat, Bernard, Grigoriev, Igor V., Martin, Francis M., and Perotto, Silvia. Comparative genomics and transcriptomics depict ericoid mycorrhizal fungi as versatile saprotrophs and plant mutualists. United States: N. p., 2018. Web. doi:10.1111/nph.14974.
Martino, Elena, Morin, Emmanuelle, Grelet, Gwen-Aëlle, Kuo, Alan, Kohler, Annegret, Daghino, Stefania, Barry, Kerrie W., Cichocki, Nicolas, Clum, Alicia, Dockter, Rhyan B., Hainaut, Matthieu, Kuo, Rita C., LaButti, Kurt, Lindahl, Björn D., Lindquist, Erika A., Lipzen, Anna, Khouja, Hassine-Radhouane, Magnuson, Jon, Murat, Claude, Ohm, Robin A., Singer, Steven W., Spatafora, Joseph W., Wang, Mei, Veneault-Fourrey, Claire, Henrissat, Bernard, Grigoriev, Igor V., Martin, Francis M., & Perotto, Silvia. Comparative genomics and transcriptomics depict ericoid mycorrhizal fungi as versatile saprotrophs and plant mutualists. United States. https://doi.org/10.1111/nph.14974
Martino, Elena, Morin, Emmanuelle, Grelet, Gwen-Aëlle, Kuo, Alan, Kohler, Annegret, Daghino, Stefania, Barry, Kerrie W., Cichocki, Nicolas, Clum, Alicia, Dockter, Rhyan B., Hainaut, Matthieu, Kuo, Rita C., LaButti, Kurt, Lindahl, Björn D., Lindquist, Erika A., Lipzen, Anna, Khouja, Hassine-Radhouane, Magnuson, Jon, Murat, Claude, Ohm, Robin A., Singer, Steven W., Spatafora, Joseph W., Wang, Mei, Veneault-Fourrey, Claire, Henrissat, Bernard, Grigoriev, Igor V., Martin, Francis M., and Perotto, Silvia. 2018. "Comparative genomics and transcriptomics depict ericoid mycorrhizal fungi as versatile saprotrophs and plant mutualists". United States. https://doi.org/10.1111/nph.14974.
@article{osti_1619093,
title = {Comparative genomics and transcriptomics depict ericoid mycorrhizal fungi as versatile saprotrophs and plant mutualists},
author = {Martino, Elena and Morin, Emmanuelle and Grelet, Gwen-Aëlle and Kuo, Alan and Kohler, Annegret and Daghino, Stefania and Barry, Kerrie W. and Cichocki, Nicolas and Clum, Alicia and Dockter, Rhyan B. and Hainaut, Matthieu and Kuo, Rita C. and LaButti, Kurt and Lindahl, Björn D. and Lindquist, Erika A. and Lipzen, Anna and Khouja, Hassine-Radhouane and Magnuson, Jon and Murat, Claude and Ohm, Robin A. and Singer, Steven W. and Spatafora, Joseph W. and Wang, Mei and Veneault-Fourrey, Claire and Henrissat, Bernard and Grigoriev, Igor V. and Martin, Francis M. and Perotto, Silvia},
abstractNote = {Some soil fungi in the Leotiomycetes form ericoid mycorrhizal (ERM) symbioses with Ericaceae. In the harsh habitats in which they occur, ERM plant survival relies on nutrient mobilization from soil organic matter (SOM) by their fungal partners. The characterization of the fungal genetic machinery underpinning both the symbiotic lifestyle and SOM degradation is needed to understand ERM symbiosis functioning and evolution, and its impact on soil carbon (C) turnover. We sequenced the genomes of the ERM fungi Meliniomyces bicolor, M. variabilis, Oidiodendron maius and Rhizoscyphus ericae, and compared their gene repertoires with those of fungi with different lifestyles (ecto- and orchid mycorrhiza, endophytes, saprotrophs, pathogens). We also identified fungal transcripts induced in symbiosis. The ERM fungal gene contents for polysaccharide-degrading enzymes, lipases, proteases and enzymes involved in secondary metabolism are closer to those of saprotrophs and pathogens than to those of ectomycorrhizal symbionts. The fungal genes most highly upregulated in symbiosis are those coding for fungal and plant cell wall-degrading enzymes (CWDEs), lipases, proteases, transporters and mycorrhiza-induced small secreted proteins (MiSSPs). The ERM fungal gene repertoire reveals a capacity for a dual saprotrophic and biotrophic lifestyle. This may reflect an incomplete transition from saprotrophy to the mycorrhizal habit, or a versatile life strategy similar to fungal endophytes.},
doi = {10.1111/nph.14974},
url = {https://www.osti.gov/biblio/1619093}, journal = {New Phytologist},
issn = {0028-646X},
number = 3,
volume = 217,
place = {United States},
year = {2018},
month = {1}
}

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