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

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:
Grant/Contract Number:
AC05-00OR22725
Type:
Accepted Manuscript
Journal Name:
Scientific Reports
Additional Journal Information:
Journal Volume: 7; Journal Issue: 1; Journal ID: ISSN 2045-2322
Publisher:
Nature Publishing Group
Research Org:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23); Australian Research Council
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
OSTI Identifier:
1351762

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., 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. 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., and Yang, Xiaohan. 2017. "Populus trichocarpa encodes small, effector-like secreted proteins that are highly induced during mutualistic symbiosis". United States. doi: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},
journal = {Scientific Reports},
number = 1,
volume = 7,
place = {United States},
year = {2017},
month = {3}
}