The Ectomycorrhizal Fungus Laccaria bicolor Produces Lipochitooligosaccharides and Uses the Common Symbiosis Pathway to Colonize Populus Roots

Cope, Kevin R.; Bascaules, Adeline; Irving, Thomas B.; Venkateshwaran, Muthusubramanian; Maeda, Junko; Garcia, Kevin; Rush, Tomás A.; Ma, Cathleen; Labbé, Jessy; Jawdy, Sara; Steigerwald, Edward; Setzke, Jonathan; Fung, Emmeline; Schnell, Kimberly G.; Wang, Yunqian; Schleif, Nathaniel; Bücking, Heike; Strauss, Steven H.; Maillet, Fabienne; Jargeat, Patricia; Bécard, Guillaume; Puech-Pagès, Virginie; Ané, Jean-Michel

doi:10.1105/tpc.18.00676

Title: The Ectomycorrhizal Fungus Laccaria bicolor Produces Lipochitooligosaccharides and Uses the Common Symbiosis Pathway to Colonize Populus Roots

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Abstract

Mycorrhizal fungi form mutualistic associations with the roots of most land plants and provide them with mineral nutrients from the soil in exchange for fixed carbon derived from photosynthesis. The common symbiosis pathway (CSP) is a conserved molecular signaling pathway in all plants capable of associating with arbuscular mycorrhizal fungi. It is required not only for arbuscular mycorrhizal symbiosis but also for rhizobia–legume and actinorhizal symbioses. Given its role in such diverse symbiotic associations, we hypothesized that the CSP also plays a role in ectomycorrhizal associations. We showed that the ectomycorrhizal fungus Laccaria bicolor produces an array of lipochitooligosaccharides (LCOs) that can trigger both root hair branching in legumes and, most importantly, calcium spiking in the host plant Populus in a CASTOR/POLLUX-dependent manner. Nonsulfated LCOs enhanced lateral root development in Populus in a calcium/calmodulin-dependent protein kinase (CCaMK)-dependent manner, and sulfated LCOs enhanced the colonization of Populus by L. bicolor. Compared with the wild-type Populus, the colonization of CASTOR/POLLUX and CCaMK RNA interference lines by L. bicolor was reduced. Our work demonstrates that similar to other root symbioses, L. bicolor uses the CSP for the full establishment of its mutualistic association with Populus.

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Department of Bacteriology, University of Wisconsin, Madison, Wisconsin 53706, Department of Agronomy, University of Wisconsin, Madison, Wisconsin 53706
Laboratoire de Recherche en Sciences Végétales, Université de Toulouse, CNRS, UPS, 31326, Castanet-Tolosan, France
Department of Agronomy, University of Wisconsin, Madison, Wisconsin 53706
Department of Forest Ecosystems and Society, Oregon State University, Corvallis, Oregon 97331
Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee 37831
Department of Bacteriology, University of Wisconsin, Madison, Wisconsin 53706
Department of Biology and Microbiology, South Dakota State University, Brookings, South Dakota 57007
Laboratoire des Interactions Plantes-Microorganismes, Université de Toulouse, INRA, CNRS, 31326, Castanet-Tolosan, France
Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee 37831, Laboratoire Evolution et Diversité Biologique, Université de Toulouse, UPS, CNRS, IRD, 31077 Toulouse, France

Publication Date:: Thu Aug 15 00:00:00 EDT 2019

Research Org.:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Org.:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

OSTI Identifier:: 1565985

Alternate Identifier(s):: OSTI ID: 1559609; OSTI ID: 1761694

Grant/Contract Number:: SC0018247; AC05-00OR22725

Resource Type:: Published Article

Journal Name:: The Plant Cell

Additional Journal Information:: Journal Name: The Plant Cell Journal Volume: 31 Journal Issue: 10; Journal ID: ISSN 1040-4651

Publisher:: Oxford University Press

Country of Publication:: United States

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES

Citation Formats


                    Cope, Kevin R., Bascaules, Adeline, Irving, Thomas B., Venkateshwaran, Muthusubramanian, Maeda, Junko, Garcia, Kevin, Rush, Tomás A., Ma, Cathleen, Labbé, Jessy, Jawdy, Sara, Steigerwald, Edward, Setzke, Jonathan, Fung, Emmeline, Schnell, Kimberly G., Wang, Yunqian, Schleif, Nathaniel, Bücking, Heike, Strauss, Steven H., Maillet, Fabienne, Jargeat, Patricia, Bécard, Guillaume, Puech-Pagès, Virginie, and Ané, Jean-Michel. The Ectomycorrhizal Fungus Laccaria bicolor Produces Lipochitooligosaccharides and Uses the Common Symbiosis Pathway to Colonize Populus Roots.  United States: N. p., 2019. 
Web.  doi:10.1105/tpc.18.00676.

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                    Cope, Kevin R., Bascaules, Adeline, Irving, Thomas B., Venkateshwaran, Muthusubramanian, Maeda, Junko, Garcia, Kevin, Rush, Tomás A., Ma, Cathleen, Labbé, Jessy, Jawdy, Sara, Steigerwald, Edward, Setzke, Jonathan, Fung, Emmeline, Schnell, Kimberly G., Wang, Yunqian, Schleif, Nathaniel, Bücking, Heike, Strauss, Steven H., Maillet, Fabienne, Jargeat, Patricia, Bécard, Guillaume, Puech-Pagès, Virginie, & Ané, Jean-Michel. The Ectomycorrhizal Fungus Laccaria bicolor Produces Lipochitooligosaccharides and Uses the Common Symbiosis Pathway to Colonize Populus Roots.  United States.  https://doi.org/10.1105/tpc.18.00676

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                    Cope, Kevin R., Bascaules, Adeline, Irving, Thomas B., Venkateshwaran, Muthusubramanian, Maeda, Junko, Garcia, Kevin, Rush, Tomás A., Ma, Cathleen, Labbé, Jessy, Jawdy, Sara, Steigerwald, Edward, Setzke, Jonathan, Fung, Emmeline, Schnell, Kimberly G., Wang, Yunqian, Schleif, Nathaniel, Bücking, Heike, Strauss, Steven H., Maillet, Fabienne, Jargeat, Patricia, Bécard, Guillaume, Puech-Pagès, Virginie, and Ané, Jean-Michel. Thu .  
"The Ectomycorrhizal Fungus Laccaria bicolor Produces Lipochitooligosaccharides and Uses the Common Symbiosis Pathway to Colonize Populus Roots".  United States.  https://doi.org/10.1105/tpc.18.00676.

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@article{osti_1565985,

  title        = {The Ectomycorrhizal Fungus Laccaria bicolor Produces Lipochitooligosaccharides and Uses the Common Symbiosis Pathway to Colonize Populus Roots},

  author       = {Cope, Kevin R. and Bascaules, Adeline and Irving, Thomas B. and Venkateshwaran, Muthusubramanian and Maeda, Junko and Garcia, Kevin and Rush, Tomás A. and Ma, Cathleen and Labbé, Jessy and Jawdy, Sara and Steigerwald, Edward and Setzke, Jonathan and Fung, Emmeline and Schnell, Kimberly G. and Wang, Yunqian and Schleif, Nathaniel and Bücking, Heike and Strauss, Steven H. and Maillet, Fabienne and Jargeat, Patricia and Bécard, Guillaume and Puech-Pagès, Virginie and Ané, Jean-Michel},

  abstractNote = {Mycorrhizal fungi form mutualistic associations with the roots of most land plants and provide them with mineral nutrients from the soil in exchange for fixed carbon derived from photosynthesis. The common symbiosis pathway (CSP) is a conserved molecular signaling pathway in all plants capable of associating with arbuscular mycorrhizal fungi. It is required not only for arbuscular mycorrhizal symbiosis but also for rhizobia–legume and actinorhizal symbioses. Given its role in such diverse symbiotic associations, we hypothesized that the CSP also plays a role in ectomycorrhizal associations. We showed that the ectomycorrhizal fungus Laccaria bicolor produces an array of lipochitooligosaccharides (LCOs) that can trigger both root hair branching in legumes and, most importantly, calcium spiking in the host plant Populus in a CASTOR/POLLUX-dependent manner. Nonsulfated LCOs enhanced lateral root development in Populus in a calcium/calmodulin-dependent protein kinase (CCaMK)-dependent manner, and sulfated LCOs enhanced the colonization of Populus by L. bicolor. Compared with the wild-type Populus, the colonization of CASTOR/POLLUX and CCaMK RNA interference lines by L. bicolor was reduced. Our work demonstrates that similar to other root symbioses, L. bicolor uses the CSP for the full establishment of its mutualistic association with Populus.},

  doi          = {10.1105/tpc.18.00676},

  journal      = {The Plant Cell},

  number       = 10,

  volume       = 31,

  place        = {United States},

  year         = {Thu Aug 15 00:00:00 EDT 2019},

  month        = {Thu Aug 15 00:00:00 EDT 2019}

}

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