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Title: Populus trichocarpa encodes small, effector-like secreted proteins that are highly induced during mutualistic symbiosis

Abstract

During symbiosis, organisms use a range of metabolic and protein-based signals to communicate. Of these protein signals, one class is defined as ‘effectors’, i.e., small secreted proteins (SSPs) that cause phenotypical and physiological changes in another organism. To date, protein-based effectors have been described in aphids, nematodes, fungi and bacteria. Using RNA sequencing of Populus trichocarpa roots in mutualistic symbiosis with the ectomycorrhizal fungus Laccaria bicolor, we sought to determine if host plants also contain genes encoding effector-like proteins. We identified 417 plant-encoded putative SSPs that were significantly regulated during this interaction, including 161 SSPs specific to P. trichocarpa and 15 SSPs exhibiting expansion in Populus and closely related lineages. We demonstrate that a subset of these SSPs can enter L. bicolor hyphae, localize to the nucleus and affect hyphal growth and morphology. Finally, we conclude that plants encode proteins that appear to function as effector proteins that may regulate symbiotic associations.

Authors:
 [1]; ORCiD logo [2]; ORCiD logo [2]; ORCiD logo [2];  [2];  [2];  [2]; ORCiD logo [2];  [3];  [3];  [3];  [2];  [4];  [5]; ORCiD logo [2]; ORCiD logo [4];  [2]; ORCiD logo [2]
  1. UMR 1136 INRA-Univ. of Lorraine, Champenoux (France); Univ. of Western Sydney, Richmond, NSW (Australia)
  2. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  3. Univ. of Tennessee, Knoxville, TN (United States)
  4. UMR 1136 INRA-Univ. of Lorraine, Champenoux (France)
  5. Univ. of Western Sydney, Richmond, NSW (Australia)
Publication Date:
Research Org.:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); Australian Research Council
OSTI Identifier:
1351762
Grant/Contract Number:  
AC05-00OR22725
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Scientific Reports
Additional Journal Information:
Journal Volume: 7; Journal Issue: 1; Journal ID: ISSN 2045-2322
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES; Populus trichocarpa; mutualistic symbiosis; small effector-like secreted proteins; biotic; plant symbiosis

Citation Formats

Plett, Jonathan M., Yin, Hengfu, Mewalal, Ritesh, Hu, Rongbin, Li, Ting, Ranjan, Priya, Jawdy, Sara, De Paoli, Henrique C., Butler, George, Burch-Smith, Tessa Maureen, Guo, Hao -Bo, Chen, Chun Ju, Kohler, Annegret, Anderson, Ian C., Labbé, Jessy L., Martin, Francis, Tuskan, Gerald A., and Yang, Xiaohan. Populus trichocarpa encodes small, effector-like secreted proteins that are highly induced during mutualistic symbiosis. United States: N. p., 2017. Web. doi:10.1038/s41598-017-00400-8.
Plett, Jonathan M., Yin, Hengfu, Mewalal, Ritesh, Hu, Rongbin, Li, Ting, Ranjan, Priya, Jawdy, Sara, De Paoli, Henrique C., Butler, George, Burch-Smith, Tessa Maureen, Guo, Hao -Bo, Chen, Chun Ju, Kohler, Annegret, Anderson, Ian C., Labbé, Jessy L., Martin, Francis, Tuskan, Gerald A., & Yang, Xiaohan. Populus trichocarpa encodes small, effector-like secreted proteins that are highly induced during mutualistic symbiosis. United States. https://doi.org/10.1038/s41598-017-00400-8
Plett, Jonathan M., Yin, Hengfu, Mewalal, Ritesh, Hu, Rongbin, Li, Ting, Ranjan, Priya, Jawdy, Sara, De Paoli, Henrique C., Butler, George, Burch-Smith, Tessa Maureen, Guo, Hao -Bo, Chen, Chun Ju, Kohler, Annegret, Anderson, Ian C., Labbé, Jessy L., Martin, Francis, Tuskan, Gerald A., and Yang, Xiaohan. 2017. "Populus trichocarpa encodes small, effector-like secreted proteins that are highly induced during mutualistic symbiosis". United States. https://doi.org/10.1038/s41598-017-00400-8. https://www.osti.gov/servlets/purl/1351762.
@article{osti_1351762,
title = {Populus trichocarpa encodes small, effector-like secreted proteins that are highly induced during mutualistic symbiosis},
author = {Plett, Jonathan M. and Yin, Hengfu and Mewalal, Ritesh and Hu, Rongbin and Li, Ting and Ranjan, Priya and Jawdy, Sara and De Paoli, Henrique C. and Butler, George and Burch-Smith, Tessa Maureen and Guo, Hao -Bo and Chen, Chun Ju and Kohler, Annegret and Anderson, Ian C. and Labbé, Jessy L. and Martin, Francis and Tuskan, Gerald A. and Yang, Xiaohan},
abstractNote = {During symbiosis, organisms use a range of metabolic and protein-based signals to communicate. Of these protein signals, one class is defined as ‘effectors’, i.e., small secreted proteins (SSPs) that cause phenotypical and physiological changes in another organism. To date, protein-based effectors have been described in aphids, nematodes, fungi and bacteria. Using RNA sequencing of Populus trichocarpa roots in mutualistic symbiosis with the ectomycorrhizal fungus Laccaria bicolor, we sought to determine if host plants also contain genes encoding effector-like proteins. We identified 417 plant-encoded putative SSPs that were significantly regulated during this interaction, including 161 SSPs specific to P. trichocarpa and 15 SSPs exhibiting expansion in Populus and closely related lineages. We demonstrate that a subset of these SSPs can enter L. bicolor hyphae, localize to the nucleus and affect hyphal growth and morphology. Finally, we conclude that plants encode proteins that appear to function as effector proteins that may regulate symbiotic associations.},
doi = {10.1038/s41598-017-00400-8},
url = {https://www.osti.gov/biblio/1351762}, journal = {Scientific Reports},
issn = {2045-2322},
number = 1,
volume = 7,
place = {United States},
year = {Thu Mar 23 00:00:00 EDT 2017},
month = {Thu Mar 23 00:00:00 EDT 2017}
}

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Cited by: 24 works
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Works referenced in this record:

Effectors in Plant–Microbe Interactions
book, November 2011


Phytophthora infestans effector AVR3a is essential for virulence and manipulates plant immunity by stabilizing host E3 ligase CMPG1
journal, May 2010


Effector MiSSP7 of the mutualistic fungus Laccaria bicolor stabilizes the Populus JAZ6 protein and represses jasmonic acid (JA) responsive genes
journal, May 2014


A Secreted Fungal Effector of Glomus intraradices Promotes Symbiotic Biotrophy
journal, July 2011


Salicylic acid modulates colonization of the root microbiome by specific bacterial taxa
journal, July 2015


Flagella-Driven Chemotaxis Towards Exudate Components Is an Important Trait for Tomato Root Colonization by Pseudomonas fluorescens
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Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi
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Characterization of the elicitor-induced biosynthesis and secretion of genistein from roots of Lupinus luteus L
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Natural roles of antimicrobial peptides in microbes, plants and animals
journal, May 2011


The Hidden Chemical Cross-Talk Between Roots and Microbes: A Proteomic Approach
journal, May 2012


Medicago truncatula symbiotic peptide NCR247 contributes to bacteroid differentiation through multiple mechanisms
journal, March 2014


Host plant peptides elicit a transcriptional response to control the Sinorhizobium meliloti cell cycle during symbiosis
journal, February 2014


Plant Peptides Govern Terminal Differentiation of Bacteria in Symbiosis
journal, February 2010


A Nodule-Specific Protein Secretory Pathway Required for Nitrogen-Fixing Symbiosis
journal, February 2010


Identification of nodule-specific cysteine-rich plant peptides in endosymbiotic bacteria
journal, March 2015


Discovery and annotation of small proteins using genomics, proteomics, and computational approaches
journal, March 2011


Expanding the repertoire of secretory peptides controlling root development with comparative genome analysis and functional assays
journal, July 2015


Small open reading frames associated with morphogenesis are hidden in plant genomes
journal, January 2013


LocTree2 predicts localization for all domains of life
journal, September 2012


Prediction of protein subcellular localization
journal, June 2006


YLoc—an interpretable web server for predicting subcellular localization
journal, May 2010


How metal-tolerant ecotypes of ectomycorrhizal fungi protect plants from heavy metal pollution
journal, January 2011


Effect of arbuscular mycorrhizal colonisation on the growth and phosphorus nutrition of Populus euramericana c.v. Ghoy
journal, November 2011


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


The rhizosphere microbiome and plant health
journal, August 2012


RXLR effector reservoir in two Phytophthora species is dominated by a single rapidly evolving superfamily with more than 700 members
journal, March 2008


The plant immune system
journal, November 2006


Pep1, a Secreted Effector Protein of Ustilago maydis, Is Required for Successful Invasion of Plant Cells
journal, February 2009


Subterfuge and Manipulation: Type III Effector Proteins of Phytopathogenic Bacteria
journal, October 2006


The Genome of Black Cottonwood, Populus trichocarpa (Torr. & Gray)
journal, September 2006


TopHat: discovering splice junctions with RNA-Seq
journal, March 2009


Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks
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Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation
journal, May 2010


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journal, November 2013


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journal, August 2005


BLAST+: architecture and applications
journal, January 2009


Population genomics of Populus trichocarpa identifies signatures of selection and adaptive trait associations
journal, August 2014


Genome resequencing reveals multiscale geographic structure and extensive linkage disequilibrium in the forest tree Populus trichocarpa
journal, August 2012


Mapping short DNA sequencing reads and calling variants using mapping quality scores
journal, November 2008


BEDTools: a flexible suite of utilities for comparing genomic features
journal, January 2010


An Importin β Protein Negatively Regulates MicroRNA Activity in Arabidopsis
journal, October 2011


Identification of eukaryotic secreted and cell surface proteins using the yeast secretion trap screen
journal, December 2006


Coriander Genomics Database: a genomic, transcriptomic, and metabolic database for coriander
journal, April 2020


Genome Sequencing of Kocuria varians Strain 80, Isolated from Starter Culture for Dry Sausage
journal, February 2021


Genomic insight into diet adaptation in the biological control agent Cryptolaemus montrouzieri
journal, February 2021


Prediction of protein subcellular localization
journal, June 2006


How metal-tolerant ecotypes of ectomycorrhizal fungi protect plants from heavy metal pollution
journal, January 2011


Effect of arbuscular mycorrhizal colonisation on the growth and phosphorus nutrition of Populus euramericana c.v. Ghoy
journal, November 2011


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


A Secreted Fungal Effector of Glomus intraradices Promotes Symbiotic Biotrophy
journal, July 2011


Natural roles of antimicrobial peptides in microbes, plants and animals
journal, May 2011


The rhizosphere microbiome and plant health
journal, August 2012


Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi
journal, June 2005


Population genomics of Populus trichocarpa identifies signatures of selection and adaptive trait associations
journal, August 2014


Identification of eukaryotic secreted and cell surface proteins using the yeast secretion trap screen
journal, December 2006


Trichoderma: a multipurpose, plant-beneficial microorganism for eco-sustainable agriculture
journal, November 2022


RXLR effector reservoir in two Phytophthora species is dominated by a single rapidly evolving superfamily with more than 700 members
journal, March 2008


Phytophthora infestans effector AVR3a is essential for virulence and manipulates plant immunity by stabilizing host E3 ligase CMPG1
journal, May 2010


Small open reading frames associated with morphogenesis are hidden in plant genomes
journal, January 2013


Effector MiSSP7 of the mutualistic fungus Laccaria bicolor stabilizes the Populus JAZ6 protein and represses jasmonic acid (JA) responsive genes
journal, May 2014


Host plant peptides elicit a transcriptional response to control the Sinorhizobium meliloti cell cycle during symbiosis
journal, February 2014


Medicago truncatula symbiotic peptide NCR247 contributes to bacteroid differentiation through multiple mechanisms
journal, March 2014


Root-Microbe Communication through Protein Secretion
journal, July 2008


TopHat: discovering splice junctions with RNA-Seq
journal, March 2009


BEDTools: a flexible suite of utilities for comparing genomic features
journal, January 2010


Characterization of the elicitor-induced biosynthesis and secretion of genistein from roots of Lupinus luteus L
journal, October 1999


Expanding the repertoire of secretory peptides controlling root development with comparative genome analysis and functional assays
journal, July 2015


YLoc—an interpretable web server for predicting subcellular localization
journal, May 2010


Pfam: the protein families database
journal, November 2013


Identification of a Protein from Rust Fungi Transferred from Haustoria into Infected Plant Cells
journal, November 2005


Mapping short DNA sequencing reads and calling variants using mapping quality scores
journal, November 2008


An Importin β Protein Negatively Regulates MicroRNA Activity in Arabidopsis
journal, October 2011


Genome resequencing reveals multiscale geographic structure and extensive linkage disequilibrium in the forest tree Populus trichocarpa
journal, August 2012


The Genome of Black Cottonwood, Populus trichocarpa (Torr. & Gray)
journal, September 2006


Salicylic acid modulates colonization of the root microbiome by specific bacterial taxa
journal, July 2015


Subterfuge and Manipulation: Type III Effector Proteins of Phytopathogenic Bacteria
journal, October 2006


BLAST+: architecture and applications
journal, January 2009


Emiliania huxleyi endures N-limitation with an efficient metabolic budgeting and effective ATP synthesis
journal, January 2014


The Hidden Chemical Cross-Talk Between Roots and Microbes: A Proteomic Approach
journal, May 2012


An Improved Filtering Algorithm for Big Read Datasets
preprint, January 2016


Works referencing / citing this record:

Plant–Microbe Symbiosis: What Has Proteomics Taught Us?
journal, August 2019


Role of antimicrobial peptides in controlling symbiotic bacterial populations
journal, January 2018


Nodule‐specific PLAT domain proteins are expanded in the Medicago lineage and required for nodulation
journal, February 2019