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:
-
- UMR 1136 INRA-Univ. of Lorraine, Champenoux (France); Univ. of Western Sydney, Richmond, NSW (Australia)
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
- Univ. of Tennessee, Knoxville, TN (United States)
- UMR 1136 INRA-Univ. of Lorraine, Champenoux (France)
- 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:
- 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. Thu .
"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},
journal = {Scientific Reports},
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}
}
Web of Science
Works referenced in this record:
Effectors in Plant–Microbe Interactions
book, November 2011
- Martin, Francis; Kamoun, Sophien
- John Wiley & Sons, Inc
Phytophthora infestans effector AVR3a is essential for virulence and manipulates plant immunity by stabilizing host E3 ligase CMPG1
journal, May 2010
- Bos, J. I. B.; Armstrong, M. R.; Gilroy, E. M.
- Proceedings of the National Academy of Sciences, Vol. 107, Issue 21
The C-terminal half of Phytophthora infestans RXLR effector AVR3a is sufficient to trigger R3a-mediated hypersensitivity and suppress INF1-induced cell death in Nicotiana benthamiana
journal, October 2006
- Bos, Jorunn I. B.; Kanneganti, Thirumala-Devi; Young, Carolyn
- The Plant Journal, Vol. 48, Issue 2
Sequential Delivery of Host-Induced Virulence Effectors by Appressoria and Intracellular Hyphae of the Phytopathogen Colletotrichum higginsianum
journal, April 2012
- Kleemann, Jochen; Rincon-Rivera, Linda J.; Takahara, Hiroyuki
- PLoS Pathogens, Vol. 8, Issue 4
A secreted Ustilago maydis effector promotes virulence by targeting anthocyanin biosynthesis in maize
journal, January 2014
- Tanaka, Shigeyuki; Brefort, Thomas; Neidig, Nina
- eLife, Vol. 3
Effector MiSSP7 of the mutualistic fungus Laccaria bicolor stabilizes the Populus JAZ6 protein and represses jasmonic acid (JA) responsive genes
journal, May 2014
- Plett, J. M.; Daguerre, Y.; Wittulsky, S.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 22
A Secreted Fungal Effector of Glomus intraradices Promotes Symbiotic Biotrophy
journal, July 2011
- Kloppholz, Silke; Kuhn, Hannah; Requena, Natalia
- Current Biology, Vol. 21, Issue 14
Salicylic acid modulates colonization of the root microbiome by specific bacterial taxa
journal, July 2015
- Lebeis, S. L.; Paredes, S. H.; Lundberg, D. S.
- Science, Vol. 349, Issue 6250
Flagella-Driven Chemotaxis Towards Exudate Components Is an Important Trait for Tomato Root Colonization by Pseudomonas fluorescens
journal, November 2002
- de Weert, Sandra; Vermeiren, Hans; Mulders, Ine H. M.
- Molecular Plant-Microbe Interactions, Vol. 15, Issue 11
Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi
journal, June 2005
- Akiyama, Kohki; Matsuzaki, Ken-ichi; Hayashi, Hideo
- Nature, Vol. 435, Issue 7043
Characterization of the elicitor-induced biosynthesis and secretion of genistein from roots of Lupinus luteus L
journal, October 1999
- Kneer, R.; Poulev, A. A.; Olesinski, A.
- Journal of Experimental Botany, Vol. 50, Issue 339
Natural roles of antimicrobial peptides in microbes, plants and animals
journal, May 2011
- Maróti, Gergely; Kereszt, Attila; Kondorosi, Éva
- Research in Microbiology, Vol. 162, Issue 4
The Hidden Chemical Cross-Talk Between Roots and Microbes: A Proteomic Approach
journal, May 2012
- De-la-Pena, Clelia; M. Loyola-Vargas, Victor
- Current Proteomics, Vol. 9, Issue 2
Structural and Functional Studies of a Phosphatidic Acid-Binding Antifungal Plant Defensin MtDef4: Identification of an RGFRRR Motif Governing Fungal Cell Entry
journal, December 2013
- Sagaram, Uma Shankar; El-Mounadi, Kaoutar; Buchko, Garry W.
- PLoS ONE, Vol. 8, Issue 12
Medicago truncatula symbiotic peptide NCR247 contributes to bacteroid differentiation through multiple mechanisms
journal, March 2014
- Farkas, A.; Maroti, G.; Durg , H.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 14
Host plant peptides elicit a transcriptional response to control the Sinorhizobium meliloti cell cycle during symbiosis
journal, February 2014
- Penterman, Jon; Abo, Ryan P.; De Nisco, Nicole J.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 9
Plant Peptides Govern Terminal Differentiation of Bacteria in Symbiosis
journal, February 2010
- Van de Velde, W.; Zehirov, G.; Szatmari, A.
- Science, Vol. 327, Issue 5969
A Nodule-Specific Protein Secretory Pathway Required for Nitrogen-Fixing Symbiosis
journal, February 2010
- Wang, D.; Griffitts, J.; Starker, C.
- Science, Vol. 327, Issue 5969
Identification of nodule-specific cysteine-rich plant peptides in endosymbiotic bacteria
journal, March 2015
- Durgo, Hajnalka; Klement, Eva; Hunyadi-Gulyas, Eva
- PROTEOMICS, Vol. 15, Issue 13
Discovery and annotation of small proteins using genomics, proteomics, and computational approaches
journal, March 2011
- Yang, X.; Tschaplinski, T. J.; Hurst, G. B.
- Genome Research, Vol. 21, Issue 4
Expanding the repertoire of secretory peptides controlling root development with comparative genome analysis and functional assays
journal, July 2015
- Ghorbani, Sarieh; Lin, Yao-Cheng; Parizot, Boris
- Journal of Experimental Botany, Vol. 66, Issue 17
Small open reading frames associated with morphogenesis are hidden in plant genomes
journal, January 2013
- Hanada, K.; Higuchi-Takeuchi, M.; Okamoto, M.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 6
LocTree2 predicts localization for all domains of life
journal, September 2012
- Goldberg, Tatyana; Hamp, Tobias; Rost, Burkhard
- Bioinformatics, Vol. 28, Issue 18
Prediction of protein subcellular localization
journal, June 2006
- Yu, Chin-Sheng; Chen, Yu-Ching; Lu, Chih-Hao
- Proteins: Structure, Function, and Bioinformatics, Vol. 64, Issue 3
YLoc—an interpretable web server for predicting subcellular localization
journal, May 2010
- Briesemeister, Sebastian; Rahnenf�hrer, J�rg; Kohlbacher, Oliver
- Nucleic Acids Research, Vol. 38, Issue suppl_2
Identification of quantitative trait loci affecting ectomycorrhizal symbiosis in an interspecific F1 poplar cross and differential expression of genes in ectomycorrhizas of the two parents: Populus deltoides and Populus trichocarpa
journal, January 2011
- Labbé, Jessy; Jorge, Véronique; Kohler, Annegret
- Tree Genetics & Genomes, Vol. 7, Issue 3
How metal-tolerant ecotypes of ectomycorrhizal fungi protect plants from heavy metal pollution
journal, January 2011
- Colpaert, Jan V.; Wevers, Jan H. L.; Krznaric, Erik
- Annals of Forest Science, Vol. 68, Issue 1
Paxillus involutus Strains MAJ and NAU Mediate K + /Na + Homeostasis in Ectomycorrhizal Populus × canescens under Sodium Chloride Stress
journal, May 2012
- Li, Jing; Bao, Siqin; Zhang, Yuhong
- Plant Physiology, Vol. 159, Issue 4
Attributing functions to ectomycorrhizal fungal identities in assemblages for nitrogen acquisition under stress
journal, September 2013
- Pena, Rodica; Polle, Andrea
- The ISME Journal, Vol. 8, Issue 2
Effect of arbuscular mycorrhizal colonisation on the growth and phosphorus nutrition of Populus euramericana c.v. Ghoy
journal, November 2011
- Rooney, D. C.; Prosser, J. I.; Bending, G. D.
- Biomass and Bioenergy, Vol. 35, Issue 11
The In Vitro Mass-Produced Model Mycorrhizal Fungus, Rhizophagus irregularis, Significantly Increases Yields of the Globally Important Food Security Crop Cassava
journal, August 2013
- Ceballos, Isabel; Ruiz, Michael; Fernández, Cristhian
- PLoS ONE, Vol. 8, Issue 8
Effects of Rhizobium, arbuscular mycorrhiza and whey applications on some properties in chickpea (Cicer arietinum L.) under irrigated and rainfed conditions 1—Yield, yield components, nodulation and AMF colonization
journal, April 2011
- Erman, Murat; Demir, Semra; Ocak, Elvan
- Field Crops Research, Vol. 122, Issue 1
A Secreted Effector Protein of Laccaria bicolor Is Required for Symbiosis Development
journal, July 2011
- Plett, Jonathan M.; Kemppainen, Minna; Kale, Shiv D.
- Current Biology, Vol. 21, Issue 14
The rhizosphere microbiome and plant health
journal, August 2012
- Berendsen, Roeland L.; Pieterse, Corné M. J.; Bakker, Peter A. H. M.
- Trends in Plant Science, Vol. 17, Issue 8
Evolutionary ecology of plant-microbe interactions: soil microbial structure alters selection on plant traits
journal, June 2011
- Lau, Jennifer A.; Lennon, Jay T.
- New Phytologist, Vol. 192, Issue 1
Comparative analysis of defence responses induced by the endophytic plant growth-promoting rhizobacterium Burkholderia phytofirmans strain PsJN and the non-host bacterium Pseudomonas syringae pv. pisi in grapevine cell suspensions
journal, September 2010
- Bordiec, S.; Paquis, S.; Lacroix, H.
- Journal of Experimental Botany, Vol. 62, Issue 2
Transcript and metabolite analysis of the Trichoderma-induced systemic resistance response to Pseudomonas syringae in Arabidopsis thaliana
journal, January 2012
- Brotman, Yariv; Lisec, Jan; Méret, Michaël
- Microbiology, Vol. 158, Issue 1
RXLR effector reservoir in two Phytophthora species is dominated by a single rapidly evolving superfamily with more than 700 members
journal, March 2008
- Jiang, R. H. Y.; Tripathy, S.; Govers, F.
- Proceedings of the National Academy of Sciences, Vol. 105, Issue 12
The plant immune system
journal, November 2006
- Jones, Jonathan D. G.; Dangl, Jeffery L.
- Nature, Vol. 444, Issue 7117
Pep1, a Secreted Effector Protein of Ustilago maydis, Is Required for Successful Invasion of Plant Cells
journal, February 2009
- Doehlemann, Gunther; van der Linde, Karina; Aßmann, Daniela
- PLoS Pathogens, Vol. 5, Issue 2
Subterfuge and Manipulation: Type III Effector Proteins of Phytopathogenic Bacteria
journal, October 2006
- Grant, Sarah R.; Fisher, Emily J.; Chang, Jeff H.
- Annual Review of Microbiology, Vol. 60, Issue 1
Effect of inoculum type and inoculation dose on ectomycorrhizal development, root necrosis and growth of Douglas fir seedlings inoculated with Laccaria laccata in a nursery
journal, January 1988
- Mortier, F.; Le Tacon, F.; Garbaye, J.
- Annales des Sciences Forestières, Vol. 45, Issue 4
The Mutualist Laccaria bicolor Expresses a Core Gene Regulon During the Colonization of Diverse Host Plants and a Variable Regulon to Counteract Host-Specific Defenses
journal, March 2015
- Plett, Jonathan M.; Tisserant, Emilie; Brun, Annick
- Molecular Plant-Microbe Interactions, Vol. 28, Issue 3
The Genome of Black Cottonwood, Populus trichocarpa (Torr. & Gray)
journal, September 2006
- Tuskan, G. A.; DiFazio, S.; Jansson, S.
- Science, Vol. 313, Issue 5793, p. 1596-1604
TopHat: discovering splice junctions with RNA-Seq
journal, March 2009
- Trapnell, Cole; Pachter, Lior; Salzberg, Steven L.
- Bioinformatics, Vol. 25, Issue 9
Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks
journal, March 2012
- Trapnell, Cole; Roberts, Adam; Goff, Loyal
- Nature Protocols, Vol. 7, Issue 3
Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation
journal, May 2010
- Trapnell, Cole; Williams, Brian A.; Pertea, Geo
- Nature Biotechnology, Vol. 28, Issue 5
Pfam: the protein families database
journal, November 2013
- Finn, Robert D.; Bateman, Alex; Clements, Jody
- Nucleic Acids Research, Vol. 42, Issue D1
Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research
journal, August 2005
- Conesa, A.; Gotz, S.; Garcia-Gomez, J. M.
- Bioinformatics, Vol. 21, Issue 18
BiNGO: a Cytoscape plugin to assess overrepresentation of Gene Ontology categories in Biological Networks
journal, June 2005
- Maere, S.; Heymans, K.; Kuiper, M.
- Bioinformatics, Vol. 21, Issue 16
BLAST+: architecture and applications
journal, January 2009
- Camacho, Christiam; Coulouris, George; Avagyan, Vahram
- BMC Bioinformatics, Vol. 10, Issue 1
Population genomics of Populus trichocarpa identifies signatures of selection and adaptive trait associations
journal, August 2014
- Evans, Luke M.; Slavov, Gancho T.; Rodgers-Melnick, Eli
- Nature Genetics, Vol. 46, Issue 10
Genome resequencing reveals multiscale geographic structure and extensive linkage disequilibrium in the forest tree Populus trichocarpa
journal, August 2012
- Slavov, Gancho T.; DiFazio, Stephen P.; Martin, Joel
- New Phytologist, Vol. 196, Issue 3, p. 713-725
Mapping short DNA sequencing reads and calling variants using mapping quality scores
journal, November 2008
- Li, H.; Ruan, J.; Durbin, R.
- Genome Research, Vol. 18, Issue 11
BEDTools: a flexible suite of utilities for comparing genomic features
journal, January 2010
- Quinlan, Aaron R.; Hall, Ira M.
- Bioinformatics, Vol. 26, Issue 6
An Importin β Protein Negatively Regulates MicroRNA Activity in Arabidopsis
journal, October 2011
- Wang, Wei; Ye, Ruiqiang; Xin, Ying
- The Plant Cell, Vol. 23, Issue 10
Identification of eukaryotic secreted and cell surface proteins using the yeast secretion trap screen
journal, December 2006
- Lee, Sang-Jik; Kim, Byung-Dong; Rose, Jocelyn K. C.
- Nature Protocols, Vol. 1, Issue 5
Coriander Genomics Database: a genomic, transcriptomic, and metabolic database for coriander
journal, April 2020
- Song, Xiaoming; Nie, Fulei; Chen, Wei
- Horticulture Research, Vol. 7, Issue 1
Genome Sequencing of Kocuria varians Strain 80, Isolated from Starter Culture for Dry Sausage
journal, February 2021
- Konorov, Evgenii A.; Kurbakov, Konstantin A.; Minaev, Mikhail Y.
- Microbiology Resource Announcements, Vol. 10, Issue 8
Genomic insight into diet adaptation in the biological control agent Cryptolaemus montrouzieri
journal, February 2021
- Li, Hao-Sen; Huang, Yu-Hao; Chen, Mei-Lan
- BMC Genomics, Vol. 22, Issue 1
Prediction of protein subcellular localization
journal, June 2006
- Yu, Chin-Sheng; Chen, Yu-Ching; Lu, Chih-Hao
- Proteins: Structure, Function, and Bioinformatics, Vol. 64, Issue 3
Identification of quantitative trait loci affecting ectomycorrhizal symbiosis in an interspecific F1 poplar cross and differential expression of genes in ectomycorrhizas of the two parents: Populus deltoides and Populus trichocarpa
journal, January 2011
- Labbé, Jessy; Jorge, Véronique; Kohler, Annegret
- Tree Genetics & Genomes, Vol. 7, Issue 3
How metal-tolerant ecotypes of ectomycorrhizal fungi protect plants from heavy metal pollution
journal, January 2011
- Colpaert, Jan V.; Wevers, Jan H. L.; Krznaric, Erik
- Annals of Forest Science, Vol. 68, Issue 1
Effect of arbuscular mycorrhizal colonisation on the growth and phosphorus nutrition of Populus euramericana c.v. Ghoy
journal, November 2011
- Rooney, D. C.; Prosser, J. I.; Bending, G. D.
- Biomass and Bioenergy, Vol. 35, Issue 11
A Secreted Effector Protein of Laccaria bicolor Is Required for Symbiosis Development
journal, July 2011
- Plett, Jonathan M.; Kemppainen, Minna; Kale, Shiv D.
- Current Biology, Vol. 21, Issue 14
A Secreted Fungal Effector of Glomus intraradices Promotes Symbiotic Biotrophy
journal, July 2011
- Kloppholz, Silke; Kuhn, Hannah; Requena, Natalia
- Current Biology, Vol. 21, Issue 14
Effects of Rhizobium, arbuscular mycorrhiza and whey applications on some properties in chickpea (Cicer arietinum L.) under irrigated and rainfed conditions 1—Yield, yield components, nodulation and AMF colonization
journal, April 2011
- Erman, Murat; Demir, Semra; Ocak, Elvan
- Field Crops Research, Vol. 122, Issue 1
Natural roles of antimicrobial peptides in microbes, plants and animals
journal, May 2011
- Maróti, Gergely; Kereszt, Attila; Kondorosi, Éva
- Research in Microbiology, Vol. 162, Issue 4
The rhizosphere microbiome and plant health
journal, August 2012
- Berendsen, Roeland L.; Pieterse, Corné M. J.; Bakker, Peter A. H. M.
- Trends in Plant Science, Vol. 17, Issue 8
Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi
journal, June 2005
- Akiyama, Kohki; Matsuzaki, Ken-ichi; Hayashi, Hideo
- Nature, Vol. 435, Issue 7043
Population genomics of Populus trichocarpa identifies signatures of selection and adaptive trait associations
journal, August 2014
- Evans, Luke M.; Slavov, Gancho T.; Rodgers-Melnick, Eli
- Nature Genetics, Vol. 46, Issue 10
Identification of eukaryotic secreted and cell surface proteins using the yeast secretion trap screen
journal, December 2006
- Lee, Sang-Jik; Kim, Byung-Dong; Rose, Jocelyn K. C.
- Nature Protocols, Vol. 1, Issue 5
Trichoderma: a multipurpose, plant-beneficial microorganism for eco-sustainable agriculture
journal, November 2022
- Woo, Sheridan L.; Hermosa, Rosa; Lorito, Matteo
- Nature Reviews Microbiology, Vol. 21, Issue 5
Effect of inoculum type and inoculation dose on ectomycorrhizal development, root necrosis and growth of Douglas fir seedlings inoculated with Laccaria laccata in a nursery
journal, January 1988
- Mortier, F.; Le Tacon, F.; Garbaye, J.
- Annales des Sciences Forestières, Vol. 45, Issue 4
RXLR effector reservoir in two Phytophthora species is dominated by a single rapidly evolving superfamily with more than 700 members
journal, March 2008
- Jiang, R. H. Y.; Tripathy, S.; Govers, F.
- Proceedings of the National Academy of Sciences, Vol. 105, Issue 12
Phytophthora infestans effector AVR3a is essential for virulence and manipulates plant immunity by stabilizing host E3 ligase CMPG1
journal, May 2010
- Bos, J. I. B.; Armstrong, M. R.; Gilroy, E. M.
- Proceedings of the National Academy of Sciences, Vol. 107, Issue 21
Small open reading frames associated with morphogenesis are hidden in plant genomes
journal, January 2013
- Hanada, K.; Higuchi-Takeuchi, M.; Okamoto, M.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 6
Effector MiSSP7 of the mutualistic fungus Laccaria bicolor stabilizes the Populus JAZ6 protein and represses jasmonic acid (JA) responsive genes
journal, May 2014
- Plett, J. M.; Daguerre, Y.; Wittulsky, S.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 22
Host plant peptides elicit a transcriptional response to control the Sinorhizobium meliloti cell cycle during symbiosis
journal, February 2014
- Penterman, Jon; Abo, Ryan P.; De Nisco, Nicole J.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 9
Medicago truncatula symbiotic peptide NCR247 contributes to bacteroid differentiation through multiple mechanisms
journal, March 2014
- Farkas, A.; Maroti, G.; Durg , H.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 14
Root-Microbe Communication through Protein Secretion
journal, July 2008
- De-la-Peña, Clelia; Lei, Zhentian; Watson, Bonnie S.
- Journal of Biological Chemistry, Vol. 283, Issue 37
TopHat: discovering splice junctions with RNA-Seq
journal, March 2009
- Trapnell, Cole; Pachter, Lior; Salzberg, Steven L.
- Bioinformatics, Vol. 25, Issue 9
BEDTools: a flexible suite of utilities for comparing genomic features
journal, January 2010
- Quinlan, Aaron R.; Hall, Ira M.
- Bioinformatics, Vol. 26, Issue 6
Characterization of the elicitor-induced biosynthesis and secretion of genistein from roots of Lupinus luteus L
journal, October 1999
- Kneer, R.; Poulev, A. A.; Olesinski, A.
- Journal of Experimental Botany, Vol. 50, Issue 339
Comparative analysis of defence responses induced by the endophytic plant growth-promoting rhizobacterium Burkholderia phytofirmans strain PsJN and the non-host bacterium Pseudomonas syringae pv. pisi in grapevine cell suspensions
journal, September 2010
- Bordiec, S.; Paquis, S.; Lacroix, H.
- Journal of Experimental Botany, Vol. 62, Issue 2
Expanding the repertoire of secretory peptides controlling root development with comparative genome analysis and functional assays
journal, July 2015
- Ghorbani, Sarieh; Lin, Yao-Cheng; Parizot, Boris
- Journal of Experimental Botany, Vol. 66, Issue 17
YLoc—an interpretable web server for predicting subcellular localization
journal, May 2010
- Briesemeister, Sebastian; Rahnenf�hrer, J�rg; Kohlbacher, Oliver
- Nucleic Acids Research, Vol. 38, Issue suppl_2
Pfam: the protein families database
journal, November 2013
- Finn, Robert D.; Bateman, Alex; Clements, Jody
- Nucleic Acids Research, Vol. 42, Issue D1
Barley Leaf Transcriptome and Metabolite Analysis Reveals New Aspects of Compatibility and Piriformospora indica –Mediated Systemic Induced Resistance to Powdery Mildew
journal, December 2011
- Molitor, Alexandra; Zajic, Doreen; Voll, Lars M.
- Molecular Plant-Microbe Interactions, Vol. 24, Issue 12
Identification of a Protein from Rust Fungi Transferred from Haustoria into Infected Plant Cells
journal, November 2005
- Kemen, Eric; Kemen, Ariane C.; Rafiqi, Maryam
- Molecular Plant-Microbe Interactions, Vol. 18, Issue 11
Transcript and metabolite analysis of the Trichoderma-induced systemic resistance response to Pseudomonas syringae in Arabidopsis thaliana
journal, January 2012
- Brotman, Yariv; Lisec, Jan; Méret, Michaël
- Microbiology, Vol. 158, Issue 1
Mapping short DNA sequencing reads and calling variants using mapping quality scores
journal, November 2008
- Li, H.; Ruan, J.; Durbin, R.
- Genome Research, Vol. 18, Issue 11
Paxillus involutus Strains MAJ and NAU Mediate K + /Na + Homeostasis in Ectomycorrhizal Populus × canescens under Sodium Chloride Stress
journal, May 2012
- Li, Jing; Bao, Siqin; Zhang, Yuhong
- Plant Physiology, Vol. 159, Issue 4
An Importin β Protein Negatively Regulates MicroRNA Activity in Arabidopsis
journal, October 2011
- Wang, Wei; Ye, Ruiqiang; Xin, Ying
- The Plant Cell, Vol. 23, Issue 10
Beech roots are simultaneously colonized by multiple genets of the ectomycorrhizal fungus Laccaria amethystina clustered in two genetic groups: POPULATION STRUCTURE OF LACCARIA AMETHYSTINA
journal, March 2012
- Hortal, S.; Trocha, L. K.; Murat, C.
- Molecular Ecology, Vol. 21, Issue 9
Evolutionary ecology of plant-microbe interactions: soil microbial structure alters selection on plant traits
journal, June 2011
- Lau, Jennifer A.; Lennon, Jay T.
- New Phytologist, Vol. 192, Issue 1
Genome resequencing reveals multiscale geographic structure and extensive linkage disequilibrium in the forest tree Populus trichocarpa
journal, August 2012
- Slavov, Gancho T.; DiFazio, Stephen P.; Martin, Joel
- New Phytologist, Vol. 196, Issue 3, p. 713-725
The Genome of Black Cottonwood, Populus trichocarpa (Torr. & Gray)
journal, September 2006
- Tuskan, G. A.; DiFazio, S.; Jansson, S.
- Science, Vol. 313, Issue 5793, p. 1596-1604
Salicylic acid modulates colonization of the root microbiome by specific bacterial taxa
journal, July 2015
- Lebeis, S. L.; Paredes, S. H.; Lundberg, D. S.
- Science, Vol. 349, Issue 6250
Subterfuge and Manipulation: Type III Effector Proteins of Phytopathogenic Bacteria
journal, October 2006
- Grant, Sarah R.; Fisher, Emily J.; Chang, Jeff H.
- Annual Review of Microbiology, Vol. 60, Issue 1
BLAST+: architecture and applications
journal, January 2009
- Camacho, Christiam; Coulouris, George; Avagyan, Vahram
- BMC Bioinformatics, Vol. 10, Issue 1
Emiliania huxleyi endures N-limitation with an efficient metabolic budgeting and effective ATP synthesis
journal, January 2014
- Rokitta, Sebastian D.; Von Dassow, Peter; Rost, Björn
- BMC Genomics, Vol. 15, Issue 1
Comparative analysis of microarray data in Arabidopsis transcriptome during compatible interactions with plant viruses
journal, May 2012
- Postnikova, Olga A.; Nemchinov, Lev G.
- Virology Journal, Vol. 9, Issue 1
Correction: Sequential Delivery of Host-Induced Virulence Effectors by Appressoria and Intracellular Hyphae of the Phytopathogen Colletotrichum higginsianum
journal, August 2012
- Kleemann, Jochen; Rincon-Rivera, Linda J.; Takahara, Hiroyuki
- PLoS Pathogens, Vol. 8, Issue 8
The In Vitro Mass-Produced Model Mycorrhizal Fungus, Rhizophagus irregularis, Significantly Increases Yields of the Globally Important Food Security Crop Cassava
journal, August 2013
- Ceballos, Isabel; Ruiz, Michael; Fernández, Cristhian
- PLoS ONE, Vol. 8, Issue 8
The Hidden Chemical Cross-Talk Between Roots and Microbes: A Proteomic Approach
journal, May 2012
- De-la-Pena, Clelia; M. Loyola-Vargas, Victor
- Current Proteomics, Vol. 9, Issue 2
An Improved Filtering Algorithm for Big Read Datasets
preprint, January 2016
- Wedemeyer, Axel; Kliemann, Lasse; Srivastav, Anand
- arXiv
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journal, August 2019
- Khatabi, Behnam; Gharechahi, Javad; Ghaffari, Mohammad Reza
- PROTEOMICS, Vol. 19, Issue 16
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journal, January 2018
- Mergaert, P.
- Natural Product Reports, Vol. 35, Issue 4
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journal, January 2019
- Wong, Johanna W. -H.; Plett, Jonathan M.
- Functional Plant Biology, Vol. 46, Issue 7
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journal, February 2019
- Trujillo, Diana I.; Silverstein, Kevin A. T.; Young, Nevin D.
- New Phytologist, Vol. 222, Issue 3