The Intracellular Scots Pine Shoot Symbiont Methylobacterium extorquens DSM13060 Aggregates around the Host Nucleus and Encodes Eukaryote-Like Proteins
Abstract
Endophytes are microbes that inhabit plant tissues without any apparent signs of infection, often fundamentally altering plant phenotypes. While endophytes are typically studied in plant roots, where they colonize the apoplast or dead cells, Methylobacterium extorquens strain DSM13060 is a facultatively intracellular symbiont of the meristematic cells of Scots pine (Pinus sylvestris L.) shoot tips. The bacterium promotes host growth and development without the production of known plant growth-stimulating factors. Our objective was to examine intracellular colonization by M. extorquens DSM13060 of Scots pine and sequence its genome to identify novel molecular mechanisms potentially involved in intracellular colonization and plant growth promotion. Reporter construct analysis of known growth promotion genes demonstrated that these were only weakly active inside the plant or not expressed at all. We found that bacterial cells accumulate near the nucleus in intact, living pine cells, pointing to host nuclear processes as the target of the symbiont’s activity. Genome analysis identified a set of eukaryote-like functions that are common as effectors in intracellular bacterial pathogens, supporting the notion of intracellular bacterial activity. These include ankyrin repeats, transcription factors, and host-defense silencing functions and may be secreted by a recently imported type IV secretion system. Potential factors involvedmore »
- Authors:
-
- Univ. of Oulu (Finland)
- Univ. of Oulu (Finland); Univ. of Eastern Finland, Kuopio (Finland)
- Univ. of California, Merced, CA (United States)
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); USDOE Joint Genome Institute (JGI), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC); Academy of Finland; Niemi Foundation; Tauno Tönning Foundation
- OSTI Identifier:
- 1626079
- Grant/Contract Number:
- AC02-05CH11231; 129852; 113607
- Resource Type:
- Accepted Manuscript
- Journal Name:
- mBio (Online)
- Additional Journal Information:
- Journal Name: mBio (Online); Journal Volume: 6; Journal Issue: 2; Journal ID: ISSN 2150-7511
- Publisher:
- American Society for Microbiology
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Microbiology
Citation Formats
Koskimäki, Janne J., Pirttilä, Anna Maria, Ihantola, Emmi-Leena, Halonen, Outi, and Frank, A. Carolin. The Intracellular Scots Pine Shoot Symbiont Methylobacterium extorquens DSM13060 Aggregates around the Host Nucleus and Encodes Eukaryote-Like Proteins. United States: N. p., 2015.
Web. doi:10.1128/mbio.00039-15.
Koskimäki, Janne J., Pirttilä, Anna Maria, Ihantola, Emmi-Leena, Halonen, Outi, & Frank, A. Carolin. The Intracellular Scots Pine Shoot Symbiont Methylobacterium extorquens DSM13060 Aggregates around the Host Nucleus and Encodes Eukaryote-Like Proteins. United States. https://doi.org/10.1128/mbio.00039-15
Koskimäki, Janne J., Pirttilä, Anna Maria, Ihantola, Emmi-Leena, Halonen, Outi, and Frank, A. Carolin. Tue .
"The Intracellular Scots Pine Shoot Symbiont Methylobacterium extorquens DSM13060 Aggregates around the Host Nucleus and Encodes Eukaryote-Like Proteins". United States. https://doi.org/10.1128/mbio.00039-15. https://www.osti.gov/servlets/purl/1626079.
@article{osti_1626079,
title = {The Intracellular Scots Pine Shoot Symbiont Methylobacterium extorquens DSM13060 Aggregates around the Host Nucleus and Encodes Eukaryote-Like Proteins},
author = {Koskimäki, Janne J. and Pirttilä, Anna Maria and Ihantola, Emmi-Leena and Halonen, Outi and Frank, A. Carolin},
abstractNote = {Endophytes are microbes that inhabit plant tissues without any apparent signs of infection, often fundamentally altering plant phenotypes. While endophytes are typically studied in plant roots, where they colonize the apoplast or dead cells, Methylobacterium extorquens strain DSM13060 is a facultatively intracellular symbiont of the meristematic cells of Scots pine (Pinus sylvestris L.) shoot tips. The bacterium promotes host growth and development without the production of known plant growth-stimulating factors. Our objective was to examine intracellular colonization by M. extorquens DSM13060 of Scots pine and sequence its genome to identify novel molecular mechanisms potentially involved in intracellular colonization and plant growth promotion. Reporter construct analysis of known growth promotion genes demonstrated that these were only weakly active inside the plant or not expressed at all. We found that bacterial cells accumulate near the nucleus in intact, living pine cells, pointing to host nuclear processes as the target of the symbiont’s activity. Genome analysis identified a set of eukaryote-like functions that are common as effectors in intracellular bacterial pathogens, supporting the notion of intracellular bacterial activity. These include ankyrin repeats, transcription factors, and host-defense silencing functions and may be secreted by a recently imported type IV secretion system. Potential factors involved in host growth include three copies of phospholipase A2, an enzyme that is rare in bacteria but implicated in a range of plant cellular processes, and proteins putatively involved in gibberellin biosynthesis. Our results describe a novel endophytic niche and create a foundation for postgenomic studies of a symbiosis with potential applications in forestry and agriculture.},
doi = {10.1128/mbio.00039-15},
journal = {mBio (Online)},
number = 2,
volume = 6,
place = {United States},
year = {Tue Mar 24 00:00:00 EDT 2015},
month = {Tue Mar 24 00:00:00 EDT 2015}
}
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Figures / Tables:
FIG 1: Transmission electron micrographs of bud cells of Scots pine displaying intracellular bacteria (b) and yeasts (y) residing near the nucleus (n). The cells are rich with dark chromoplasts (c). Scale bar, 2 μm.
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Works referenced in this record:
Genome Erosion in a Nitrogen-Fixing Vertically Transmitted Endosymbiotic Multicellular Cyanobacterium
journal, July 2010
- Ran, Liang; Larsson, John; Vigil-Stenman, Theoden
- PLoS ONE, Vol. 5, Issue 7
Biology and Biochemistry of Plant Phospholipases
journal, May 2011
- Chen, Guanqun; Snyder, Crystal L.; Greer, Michael S.
- Critical Reviews in Plant Sciences, Vol. 30, Issue 3
Bacterial volatiles promote growth in Arabidopsis
journal, April 2003
- Ryu, C. -M.; Farag, M. A.; Hu, C. -H.
- Proceedings of the National Academy of Sciences, Vol. 100, Issue 8
Protein Kinase G from Pathogenic Mycobacteria Promotes Survival Within Macrophages
journal, June 2004
- Walburger, A.
- Science, Vol. 304, Issue 5678
Bud endophytes of Scots pine produce adenine derivatives and other compounds that affect morphology and mitigate browning of callus cultures
journal, June 2004
- Pirttila, Anna Maria; Joensuu, Paivi; Pospiech, Helmut
- Physiologia Plantarum, Vol. 121, Issue 2
Extreme genome reduction in symbiotic bacteria
journal, November 2011
- McCutcheon, John P.; Moran, Nancy A.
- Nature Reviews Microbiology, Vol. 10, Issue 1
Distribution of genes involved in sialic acid utilization in strains of Haemophilus parasuis
journal, August 2012
- Martínez-Moliner, Verónica; Soler-Llorens, Pedro; Moleres, Javier
- Microbiology, Vol. 158, Issue 8
Properties of bacterial endophytes and their proposed role in plant growth
journal, October 2008
- Hardoim, Pablo R.; van Overbeek, Leo S.; Elsas, Jan Dirk van
- Trends in Microbiology, Vol. 16, Issue 10
Rhizobium cellulase CelC2 is essential for primary symbiotic infection of legume host roots
journal, May 2008
- Robledo, M.; Jimenez-Zurdo, J. I.; Velazquez, E.
- Proceedings of the National Academy of Sciences, Vol. 105, Issue 19
Role of Rhizobium endoglucanase CelC2 in cellulose biosynthesis and biofilm formation on plant roots and abiotic surfaces
journal, January 2012
- Robledo, M.; Rivera, L.; Jiménez-Zurdo, Jose I.
- Microbial Cell Factories, Vol. 11, Issue 1
Legume pectate lyase required for root infection by rhizobia
journal, December 2011
- Xie, F.; Murray, J. D.; Kim, J.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 2
Identification of Catalytic Residues in Glyoxal Oxidase by Targeted Mutagenesis
journal, December 1999
- Whittaker, Mei M.; Kersten, Philip J.; Cullen, Daniel
- Journal of Biological Chemistry, Vol. 274, Issue 51
Conservation and Diversity of Seed Associated Endophytes in Zea across Boundaries of Evolution, Ethnography and Ecology
journal, June 2011
- Johnston-Monje, David; Raizada, Manish N.
- PLoS ONE, Vol. 6, Issue 6
Complete Genome Sequences of Six Strains of the Genus Methylobacterium
journal, August 2012
- Marx, C. J.; Bringel, F.; Chistoserdova, L.
- Journal of Bacteriology, Vol. 194, Issue 17
Endophytic bacteria in plant tissue culture: differences between easy- and difficult-to-propagate Prunus avium genotypes
journal, May 2014
- Quambusch, M.; Pirttila, A. M.; Tejesvi, M. V.
- Tree Physiology, Vol. 34, Issue 5
Bacterial endophytes from seeds of Norway spruce ( Picea abies L. Karst)
journal, March 2005
- Cankar, Katarina; Kraigher, Hojka; Ravnikar, Maja
- FEMS Microbiology Letters, Vol. 244, Issue 2
When bacteria target the nucleus: the emerging family of nucleomodulins: Bacterial hijacking of the nucleus
journal, February 2012
- Bierne, Hélène; Cossart, Pascale
- Cellular Microbiology, Vol. 14, Issue 5
The ABCs of plasmid replication and segregation
journal, October 2012
- Pinto, Uelinton M.; Pappas, Katherine M.; Winans, Stephen C.
- Nature Reviews Microbiology, Vol. 10, Issue 11
Pseudomonas putida KT2440 causes induced systemic resistance and changes in Arabidopsis root exudation: Phytoprotection by Pseudomonas putida
journal, November 2009
- Matilla, Miguel A.; Ramos, Juan L.; Bakker, Peter A. H. M.
- Environmental Microbiology Reports, Vol. 2, Issue 3
The ankyrin repeat as molecular architecture for protein recognition
journal, June 2004
- Mosavi, Leila K.; Cammett, Tobin J.; Desrosiers, Daniel C.
- Protein Science, Vol. 13, Issue 6
Bacteriophytochrome controls photosystem synthesis in anoxygenic bacteria
journal, May 2002
- Giraud, Eric; Fardoux, Joël; Fourrier, Nicolas
- Nature, Vol. 417, Issue 6885
RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models
journal, August 2006
- Stamatakis, Alexandros
- Bioinformatics, Vol. 22, Issue 21
ProtTest: selection of best-fit models of protein evolution
journal, January 2005
- Abascal, F.; Zardoya, R.; Posada, D.
- Bioinformatics, Vol. 21, Issue 9
Evolutionary microbial genomics: insights into bacterial host adaptation
journal, June 2010
- Toft, Christina; Andersson, Siv G. E.
- Nature Reviews Genetics, Vol. 11, Issue 7
Calcium and Signal Transduction in Plants
journal, January 1993
- Poovaiah, B. W.; Reddy, A. S. N.; Feldman, Lewis
- Critical Reviews in Plant Sciences, Vol. 12, Issue 3
Widespread occurrence of an intranuclear bacterial parasite in vent and seep bathymodiolin mussels
journal, May 2009
- Zielinski, Frank U.; Pernthaler, Annelie; Duperron, Sébastien
- Environmental Microbiology, Vol. 11, Issue 5
The Legionella pneumophila icm locus: a set of genes required for intracellular multiplication in human macrophages
journal, November 1994
- Brand, Bettina C.; Sadosky, Alesia B.; Shuman, Howard A.
- Molecular Microbiology, Vol. 14, Issue 4
BRS1, a serine carboxypeptidase, regulates BRI1 signaling in Arabidopsis thaliana
journal, April 2001
- Li, J.; Lease, K. A.; Tax, F. E.
- Proceedings of the National Academy of Sciences, Vol. 98, Issue 10
Modulation of Host Cell Function by Legionella pneumophila Type IV Effectors
journal, November 2010
- Hubber, Andree; Roy, Craig R.
- Annual Review of Cell and Developmental Biology, Vol. 26, Issue 1
DNA Topoisomerases Maintain Promoters in a State Competent for Transcriptional Activation in Saccharomyces cerevisiae
journal, December 2012
- Pedersen, Jakob Madsen; Fredsoe, Jacob; Roedgaard, Morten
- PLoS Genetics, Vol. 8, Issue 12
Infection and Colonization of Sugar Cane and Other Graminaceous Plants by Endophytic Diazotrophs
journal, January 1998
- James, E.
- Critical Reviews in Plant Sciences, Vol. 17, Issue 1
Role of Protein Phosphorylation on Serine/Threonine and Tyrosine in the Virulence of Bacterial Pathogens
journal, January 2005
- Cozzone, Alain J.
- Journal of Molecular Microbiology and Biotechnology, Vol. 9, Issue 3-4
The Pfam Protein Families Database
journal, January 2000
- Bateman, A.
- Nucleic Acids Research, Vol. 28, Issue 1
Phospholipase activity during plant growth and development and in response to environmental stress
journal, November 1998
- Chapman, Kent D.
- Trends in Plant Science, Vol. 3, Issue 11
Modulation of plant ethylene levels by the bacterial enzyme ACC deaminase
journal, October 2005
- Glick, Bernard R.
- FEMS Microbiology Letters, Vol. 251, Issue 1
Cyclomodulins: bacterial effectors that modulate the eukaryotic cell cycle
journal, March 2005
- Nougayrède, Jean-Philippe; Taieb, Frédéric; Rycke, Jean De
- Trends in Microbiology, Vol. 13, Issue 3
Vitamin B12 Production by a Methanol-Utilizing Bacterium
journal, January 1975
- Toraya, Tetsuo; Yongsmith, Busaba; Tanaka, Atsuo
- Applied Microbiology, Vol. 30, Issue 3
Symbiotic use of pathogenic strategies: rhizobial protein secretion systems
journal, March 2009
- Deakin, William J.; Broughton, William J.
- Nature Reviews Microbiology, Vol. 7, Issue 4
Differential response of the plant Medicago truncatula to its symbiont Sinorhizobium meliloti or an exopolysaccharide-deficient mutant
journal, January 2008
- Jones, K. M.; Sharopova, N.; Lohar, D. P.
- Proceedings of the National Academy of Sciences, Vol. 105, Issue 2
A proteomic study of Methylobacterium extorquens reveals a response regulator essential for epiphytic growth
journal, August 2006
- Gourion, B.; Rossignol, M.; Vorholt, J. A.
- Proceedings of the National Academy of Sciences, Vol. 103, Issue 35
Gibberellin Metabolism and its Regulation
journal, June 2008
- Yamaguchi, Shinjiro
- Annual Review of Plant Biology, Vol. 59, Issue 1
Brassinosteroid Signaling Pathway
journal, November 2006
- Belkhadir, Y.; Wang, X.; Chory, J.
- Science's STKE, Vol. 2006, Issue 364
Why Genes Evolve Faster on Secondary Chromosomes in Bacteria
journal, April 2010
- Cooper, Vaughn S.; Vohr, Samuel H.; Wrocklage, Sarah C.
- PLoS Computational Biology, Vol. 6, Issue 4
Interaction with ectomycorrhizal fungi and endophytic Methylobacterium affects nutrient uptake and growth of pine seedlings in vitro
journal, August 2014
- Pohjanen, J.; Koskimaki, J. J.; Sutela, S.
- Tree Physiology, Vol. 34, Issue 9
Apoptosis: Identification of dying cells
journal, March 1998
- Renvoizé, C.; Biola, A.; Pallardy, M.
- Cell Biology and Toxicology, Vol. 14, Issue 2, p. 111-120
Comparison of the ‘Ca. Liberibacter asiaticus’ Genome Adapted for an Intracellular Lifestyle with Other Members of the Rhizobiales
journal, August 2011
- Hartung, John S.; Shao, Jonathan; Kuykendall, L. David
- PLoS ONE, Vol. 6, Issue 8
MUSCLE: a multiple sequence alignment method with reduced time and space complexity
journal, August 2004
- Edgar, Robert C.
- BMC Bioinformatics, Vol. 5, Issue 1, p. 113
Bacterial effectors target the plant cell nucleus to subvert host transcription
journal, February 2012
- Canonne, Joanne; Rivas, Susana
- Plant Signaling & Behavior, Vol. 7, Issue 2
Intracellular colonization of roots of Arabidopsis and crop plants by Gluconacetobacter diazotrophicus
journal, January 2006
- Cocking, Edward C.; Stone, Philip J.; Davey, Michael R.
- In Vitro Cellular & Developmental Biology - Plant, Vol. 42, Issue 1
Bacterial Effector Activates Jasmonate Signaling by Directly Targeting JAZ Transcriptional Repressors
journal, October 2013
- Jiang, Shushu; Yao, Jian; Ma, Ka-Wai
- PLoS Pathogens, Vol. 9, Issue 10
The interconversion of ACC deaminase and d-cysteine desulfhydrase by directed mutagenesis
journal, September 2008
- Todorovic, Biljana; Glick, Bernard R.
- Planta, Vol. 229, Issue 1
Determination of ACC-induced cell-programmed death in roots of Vicia faba ssp. minor seedlings by acridine orange and ethidium bromide staining
journal, February 2012
- Byczkowska, Anna; Kunikowska, Anita; Kaźmierczak, Andrzej
- Protoplasma, Vol. 250, Issue 1
Two Endophytic Fungi in Different Tissues of Scots Pine Buds (Pinus sylvestris L.)
journal, January 2003
- Pirttil�, A. M.; Pospiech, H.; Laukkanen, H.
- Microbial Ecology, Vol. 45, Issue 1
Bacterial SET domain proteins and their role in eukaryotic chromatin modification
journal, April 2014
- Alvarez-Venegas, Raúl
- Frontiers in Genetics, Vol. 5
Bacterial Endophytes and Their Interactions with Hosts
journal, August 2006
- Rosenblueth, Mónica; Martínez-Romero, Esperanza
- Molecular Plant-Microbe Interactions, Vol. 19, Issue 8
Photosynthetic Bradyrhizobia Are Natural Endophytes of the African Wild Rice Oryza breviligulata
journal, December 2000
- Chaintreuil, Cl�mence; Giraud, Eric; Prin, Yves
- Applied and Environmental Microbiology, Vol. 66, Issue 12
Comparative genome analysis of Burkholderia phytofirmans PsJN reveals a wide spectrum of endophytic lifestyles based on interaction strategies with host plants
journal, January 2013
- Mitter, Birgit; Petric, Alexandra; Shin, Maria W.
- Frontiers in Plant Science, Vol. 4
Genome Sequence of an Obligate Intracellular Pathogen of Humans: Chlamydia trachomatis
journal, October 1998
- Stephens, R. S.
- Science, Vol. 282, Issue 5389
Effect of Bradyrhizobium photosynthesis on stem nodulation of Aeschynomene sensitiva
journal, December 2000
- Giraud, E.; Hannibal, L.; Fardoux, J.
- Proceedings of the National Academy of Sciences, Vol. 97, Issue 26
Life in an unusual intracellular niche: a bacterial symbiont infecting the nucleus of amoebae
journal, February 2014
- Schulz, Frederik; Lagkouvardos, Ilias; Wascher, Florian
- The ISME Journal, Vol. 8, Issue 8
The eroded genome of a Psychotria leaf symbiont: hypotheses about lifestyle and interactions with its plant host: Psychotria kirkii symbiont genome
journal, May 2012
- Carlier, Aurelien L.; Eberl, Leo
- Environmental Microbiology, Vol. 14, Issue 10
Detection of Intracellular Bacteria in the Buds of Scotch Pine (Pinus sylvestris L.) by In Situ Hybridization
journal, July 2000
- Pirttil�, Anna Maria; Laukkanen, Hanna; Pospiech, Helmut
- Applied and Environmental Microbiology, Vol. 66, Issue 7
Salipiger mucescens gen. nov., sp. nov., a moderately halophilic, exopolysaccharide-producing bacterium isolated from hypersaline soil, belonging to the -Proteobacteria
journal, September 2004
- Martinez-Canovas, M. J.
- INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 54, Issue 5
Comparative Genomics Reveals Insight into Virulence Strategies of Plant Pathogenic Oomycetes
journal, October 2013
- Adhikari, Bishwo N.; Hamilton, John P.; Zerillo, Marcelo M.
- PLoS ONE, Vol. 8, Issue 10
Seasonal variations in location and population structure of endophytes in buds of Scots pine
journal, March 2005
- Pirttila, A. M.; Pospiech, H.; Laukkanen, H.
- Tree Physiology, Vol. 25, Issue 3
tRNA Is the Source of Low-Level trans-Zeatin Production in Methylobacterium spp.
journal, April 2002
- Koenig, Robbin L.; Morris, Roy O.; Polacco, Joe C.
- Journal of Bacteriology, Vol. 184, Issue 7
Methylobacterium Genome Sequences: A Reference Blueprint to Investigate Microbial Metabolism of C1 Compounds from Natural and Industrial Sources
journal, May 2009
- Vuilleumier, Stéphane; Chistoserdova, Ludmila; Lee, Ming-Chun
- PLoS ONE, Vol. 4, Issue 5
Vitamin B 12 Production by a Methanol-Utilizing Bacterium
journal, September 1975
- Toraya, Tetsuo; Yongsmith, Busaba; Tanaka, Atsuo
- Applied Microbiology, Vol. 30, Issue 3
Endophytic Bacteria in Tree Shoot Tissues and Their Effects on Host
book, January 2011
- Pirttilä, Anna Maria
- Endophytes of Forest Trees
The interconversion of ACC deaminase and d-cysteine desulfhydrase by directed mutagenesis
journal, September 2008
- Todorovic, Biljana; Glick, Bernard R.
- Planta, Vol. 229, Issue 1
Determination of ACC-induced cell-programmed death in roots of Vicia faba ssp. minor seedlings by acridine orange and ethidium bromide staining
journal, February 2012
- Byczkowska, Anna; Kunikowska, Anita; Kaźmierczak, Andrzej
- Protoplasma, Vol. 250, Issue 1
Cyclomodulins: bacterial effectors that modulate the eukaryotic cell cycle
journal, March 2005
- Nougayrède, Jean-Philippe; Taieb, Frédéric; Rycke, Jean De
- Trends in Microbiology, Vol. 13, Issue 3
Properties of bacterial endophytes and their proposed role in plant growth
journal, October 2008
- Hardoim, Pablo R.; van Overbeek, Leo S.; Elsas, Jan Dirk van
- Trends in Microbiology, Vol. 16, Issue 10
Bacteriophytochrome controls photosystem synthesis in anoxygenic bacteria
journal, May 2002
- Giraud, Eric; Fardoux, Joël; Fourrier, Nicolas
- Nature, Vol. 417, Issue 6885
Evolutionary microbial genomics: insights into bacterial host adaptation
journal, June 2010
- Toft, Christina; Andersson, Siv G. E.
- Nature Reviews Genetics, Vol. 11, Issue 7
Extreme genome reduction in symbiotic bacteria
journal, November 2011
- McCutcheon, John P.; Moran, Nancy A.
- Nature Reviews Microbiology, Vol. 10, Issue 1
Genetic basis for the establishment of endosymbiosis in Paramecium
journal, January 2019
- He, Ming; Wang, Jinfeng; Fan, Xinpeng
- The ISME Journal, Vol. 13, Issue 5
A proteomic study of Methylobacterium extorquens reveals a response regulator essential for epiphytic growth
journal, August 2006
- Gourion, B.; Rossignol, M.; Vorholt, J. A.
- Proceedings of the National Academy of Sciences, Vol. 103, Issue 35
Differential response of the plant Medicago truncatula to its symbiont Sinorhizobium meliloti or an exopolysaccharide-deficient mutant
journal, January 2008
- Jones, K. M.; Sharopova, N.; Lohar, D. P.
- Proceedings of the National Academy of Sciences, Vol. 105, Issue 2
Bacterial volatiles promote growth in Arabidopsis
journal, April 2003
- Ryu, C. -M.; Farag, M. A.; Hu, C. -H.
- Proceedings of the National Academy of Sciences, Vol. 100, Issue 8
Rhizobium cellulase CelC2 is essential for primary symbiotic infection of legume host roots
journal, May 2008
- Robledo, M.; Jimenez-Zurdo, J. I.; Velazquez, E.
- Proceedings of the National Academy of Sciences, Vol. 105, Issue 19
Legume pectate lyase required for root infection by rhizobia
journal, December 2011
- Xie, F.; Murray, J. D.; Kim, J.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 2
Effect of Bradyrhizobium photosynthesis on stem nodulation of Aeschynomene sensitiva
journal, December 2000
- Giraud, E.; Hannibal, L.; Fardoux, J.
- Proceedings of the National Academy of Sciences, Vol. 97, Issue 26
Calcium and Signal Transduction in Plants
journal, January 1993
- Poovaiah, B. W.; Reddy, A. S. N.; Feldman, Lewis
- Critical Reviews in Plant Sciences, Vol. 12, Issue 3
ProtTest: selection of best-fit models of protein evolution
journal, January 2005
- Abascal, F.; Zardoya, R.; Posada, D.
- Bioinformatics, Vol. 21, Issue 9
The Pfam Protein Families Database
journal, January 2000
- Bateman, A.
- Nucleic Acids Research, Vol. 28, Issue 1
Seasonal variations in location and population structure of endophytes in buds of Scots pine
journal, March 2005
- Pirttila, A. M.; Pospiech, H.; Laukkanen, H.
- Tree Physiology, Vol. 25, Issue 3
Endophytic bacteria in plant tissue culture: differences between easy- and difficult-to-propagate Prunus avium genotypes
journal, May 2014
- Quambusch, M.; Pirttila, A. M.; Tejesvi, M. V.
- Tree Physiology, Vol. 34, Issue 5
Interaction with ectomycorrhizal fungi and endophytic Methylobacterium affects nutrient uptake and growth of pine seedlings in vitro
journal, August 2014
- Pohjanen, J.; Koskimaki, J. J.; Sutela, S.
- Tree Physiology, Vol. 34, Issue 9
Salipiger mucescens gen. nov., sp. nov., a moderately halophilic, exopolysaccharide-producing bacterium isolated from hypersaline soil, belonging to the -Proteobacteria
journal, September 2004
- Martinez-Canovas, M. J.
- INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 54, Issue 5
Distribution of genes involved in sialic acid utilization in strains of Haemophilus parasuis
journal, August 2012
- Martínez-Moliner, Verónica; Soler-Llorens, Pedro; Moleres, Javier
- Microbiology, Vol. 158, Issue 8
Bud endophytes of Scots pine produce adenine derivatives and other compounds that affect morphology and mitigate browning of callus cultures
journal, June 2004
- Pirttila, Anna Maria; Joensuu, Paivi; Pospiech, Helmut
- Physiologia Plantarum, Vol. 121, Issue 2
Widespread occurrence of an intranuclear bacterial parasite in vent and seep bathymodiolin mussels
journal, May 2009
- Zielinski, Frank U.; Pernthaler, Annelie; Duperron, Sébastien
- Environmental Microbiology, Vol. 11, Issue 5
The eroded genome of a Psychotria leaf symbiont: hypotheses about lifestyle and interactions with its plant host: Psychotria kirkii symbiont genome
journal, May 2012
- Carlier, Aurelien L.; Eberl, Leo
- Environmental Microbiology, Vol. 14, Issue 10
When bacteria target the nucleus: the emerging family of nucleomodulins: Bacterial hijacking of the nucleus
journal, February 2012
- Bierne, Hélène; Cossart, Pascale
- Cellular Microbiology, Vol. 14, Issue 5
Genome Sequence of an Obligate Intracellular Pathogen of Humans: Chlamydia trachomatis
journal, October 1998
- Stephens, R. S.
- Science, Vol. 282, Issue 5389
Brassinosteroid Signaling Pathway
journal, November 2006
- Belkhadir, Y.; Wang, X.; Chory, J.
- Science's STKE, Vol. 2006, Issue 364
Modulation of Host Cell Function by Legionella pneumophila Type IV Effectors
journal, November 2010
- Hubber, Andree; Roy, Craig R.
- Annual Review of Cell and Developmental Biology, Vol. 26, Issue 1
Gibberellin Metabolism and its Regulation
journal, June 2008
- Yamaguchi, Shinjiro
- Annual Review of Plant Biology, Vol. 59, Issue 1
Role of Protein Phosphorylation on Serine/Threonine and Tyrosine in the Virulence of Bacterial Pathogens
journal, January 2005
- Cozzone, Alain J.
- Journal of Molecular Microbiology and Biotechnology, Vol. 9, Issue 3-4
Role of Rhizobium endoglucanase CelC2 in cellulose biosynthesis and biofilm formation on plant roots and abiotic surfaces
journal, January 2012
- Robledo, M.; Rivera, L.; Jiménez-Zurdo, Jose I.
- Microbial Cell Factories, Vol. 11, Issue 1
Why Genes Evolve Faster on Secondary Chromosomes in Bacteria
journal, April 2010
- Cooper, Vaughn S.; Vohr, Samuel H.; Wrocklage, Sarah C.
- PLoS Computational Biology, Vol. 6, Issue 4
DNA Topoisomerases Maintain Promoters in a State Competent for Transcriptional Activation in Saccharomyces cerevisiae
journal, December 2012
- Pedersen, Jakob Madsen; Fredsoe, Jacob; Roedgaard, Morten
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Comparative Genomics Reveals Insight into Virulence Strategies of Plant Pathogenic Oomycetes
journal, October 2013
- Adhikari, Bishwo N.; Hamilton, John P.; Zerillo, Marcelo M.
- PLoS ONE, Vol. 8, Issue 10
Bacterial Effector Activates Jasmonate Signaling by Directly Targeting JAZ Transcriptional Repressors
journal, October 2013
- Jiang, Shushu; Yao, Jian; Ma, Ka-Wai
- PLoS Pathogens, Vol. 9, Issue 10
Bacterial SET domain proteins and their role in eukaryotic chromatin modification
journal, April 2014
- Alvarez-Venegas, Raúl
- Frontiers in Genetics, Vol. 5
Comparative genome analysis of Burkholderia phytofirmans PsJN reveals a wide spectrum of endophytic lifestyles based on interaction strategies with host plants
journal, January 2013
- Mitter, Birgit; Petric, Alexandra; Shin, Maria W.
- Frontiers in Plant Science, Vol. 4
Methylobacterium Genome Sequences: A Reference Blueprint to Investigate Microbial Metabolism of C1 Compounds from Natural and Industrial Sources
text, January 2009
- Vuilleumier, Stéphane; Chistoserdova, Ludmila; Lee, Ming-Chun
- ETH Zurich
Bacterial effectors target the plant cell nucleus to subvert host transcription
journal, February 2012
- Canonne, Joanne; Rivas, Susana
- Plant Signaling & Behavior, Vol. 7, Issue 2
Protein kinase G from pathogenic mycobacteria promotes survival within macrophages
text, January 2004
- A., Walburger,; A., Koul,; G., Ferrari,
- American Association for the Advancement of Science
Works referencing / citing this record:
Nitrogen Fixing Endophytes in Forest Trees
book, January 2018
- Oses, Rómulo; Frank, A. Carolin; Valenzuela, Sofía
- Endophytes of Forest Trees
Ribosome Incorporation into Somatic Cells Promotes Lineage Transdifferentiation towards Multipotency
journal, January 2018
- Ito, Naofumi; Katoh, Kaoru; Kushige, Hiroko
- Scientific Reports, Vol. 8, Issue 1
Methyl-esterified 3-hydroxybutyrate oligomers protect bacteria from hydroxyl radicals
journal, March 2016
- Koskimäki, Janne J.; Kajula, Marena; Hokkanen, Juho
- Nature Chemical Biology, Vol. 12, Issue 5
Bioactive Products From Plant-Endophytic Gram-Positive Bacteria
journal, March 2019
- Ek-Ramos, María J.; Gomez-Flores, Ricardo; Orozco-Flores, Alonso A.
- Frontiers in Microbiology, Vol. 10
Leaf-residing Methylobacterium species fix nitrogen and promote biomass and seed production in Jatropha curcas
journal, December 2015
- Madhaiyan, Munusamy; Alex, Tan Hian Hwee; Ngoh, Si Te
- Biotechnology for Biofuels, Vol. 8, Issue 1
Inner Plant Values: Diversity, Colonization and Benefits from Endophytic Bacteria
journal, December 2017
- Liu, Hongwei; Carvalhais, Lilia C.; Crawford, Mark
- Frontiers in Microbiology, Vol. 8
Transmission of Bacterial Endophytes
journal, November 2017
- Frank, Anna; Saldierna Guzmán, Jessica; Shay, Jackie
- Microorganisms, Vol. 5, Issue 4
Plant Microbiome Innovation: M-trophs
journal, June 2018
- Laurita, Thomas; Kerovuo, Janne
- Industrial Biotechnology, Vol. 14, Issue 3
Associations between Ectomycorrhizal Fungi and Bacterial Needle Endophytes in Pinus radiata: Implications for Biotic Selection of Microbial Communities
journal, March 2016
- Rúa, Megan A.; Wilson, Emily C.; Steele, Sarah
- Frontiers in Microbiology, Vol. 7
Inner Plant Values: Diversity, Colonization and Benefits from Endophytic Bacteria
journal, December 2017
- Liu, Hongwei; Carvalhais, Lilia C.; Crawford, Mark
- Frontiers in Microbiology, Vol. 8
Transmission of Bacterial Endophytes
journal, November 2017
- Frank, Anna; Saldierna Guzmán, Jessica; Shay, Jackie
- Microorganisms, Vol. 5, Issue 4
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