Genomic Changes Associated with the Evolutionary Transitions of Nostoc to a Plant Symbiont
Abstract
Cyanobacteria belonging to the genus Nostoc comprise free-living strains and also facultative plant symbionts. Symbiotic strains can enter into symbiosis with taxonomically diverse range of host plants. Little is known about genomic changes associated with evolutionary transition of Nostoc from free-living to plant symbiont. Here, we compared the genomes derived from 11 symbiotic Nostoc strains isolated from different host plants and infer phylogenetic relationships between strains. Phylogenetic reconstructions of 89 Nostocales showed that symbiotic Nostoc strains with a broad host range, entering epiphytic and intracellular or extracellular endophytic interactions, form a monophyletic clade indicating a common evolutionary history. A polyphyletic origin was found for Nostoc strains which enter only extracellular symbioses, and inference of transfer events implied that this trait was likely acquired several times in the evolution of the Nostocales. Symbiotic Nostoc strains showed enriched functions in transport and metabolism of organic sulfur, chemotaxis and motility, as well as the uptake of phosphate, branched-chain amino acids, and ammonium. The genomes of the intracellular clade differ from that of other Nostoc strains, with a gain/enrichment of genes encoding proteins to generate L-methionine from sulfite and pathways for the degradation of the plant metabolites vanillin and vanillate, and of the macromoleculemore »
- Authors:
-
[1];
[1];
- Department of Ecology, Environment and Plant Sciences, Stockholm University, Stockholm, Sweden
- Department of Arctic and Marine Biology, Faculty of Biosciences, Fisheries and Economics, UiT–The Arctic University of Norway, Tromsø, Norway
- US Department of Energy Joint Genome Institute, Walnut Creek, CA
- Department of Chemistry, Faculty of Science and Technology, UiT–The Arctic University of Norway, Tromsø, Norway
- Department of Synthetic Biology and Bioenergy, J. Craig Venter Institute, La Jolla, CA
- Department of Microbial and Environmental Genomics, J. Craig Venter Institute, La Jolla, CA
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC); Univ. of California, Oakland, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1434367
- Alternate Identifier(s):
- OSTI ID: 1543986
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Published Article
- Journal Name:
- Molecular Biology and Evolution
- Additional Journal Information:
- Journal Name: Molecular Biology and Evolution Journal Volume: 35 Journal Issue: 5; Journal ID: ISSN 0737-4038
- Publisher:
- Oxford University Press
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Biochemistry & Molecular Biology; Evolutionary Biology; Genetics & Heredity; cyanobacteria; symbiosis; evolution; plant–microbe interaction
Citation Formats
Warshan, Denis, Liaimer, Anton, Pederson, Eric, Kim, Sea-Yong, Shapiro, Nicole, Woyke, Tanja, Altermark, Bjørn, Pawlowski, Katharina, Weyman, Philip D., Dupont, Christopher L., Rasmussen, Ulla, and Perna, ed., Nicole. Genomic Changes Associated with the Evolutionary Transitions of Nostoc to a Plant Symbiont. United States: N. p., 2018.
Web. doi:10.1093/molbev/msy029.
Warshan, Denis, Liaimer, Anton, Pederson, Eric, Kim, Sea-Yong, Shapiro, Nicole, Woyke, Tanja, Altermark, Bjørn, Pawlowski, Katharina, Weyman, Philip D., Dupont, Christopher L., Rasmussen, Ulla, & Perna, ed., Nicole. Genomic Changes Associated with the Evolutionary Transitions of Nostoc to a Plant Symbiont. United States. https://doi.org/10.1093/molbev/msy029
Warshan, Denis, Liaimer, Anton, Pederson, Eric, Kim, Sea-Yong, Shapiro, Nicole, Woyke, Tanja, Altermark, Bjørn, Pawlowski, Katharina, Weyman, Philip D., Dupont, Christopher L., Rasmussen, Ulla, and Perna, ed., Nicole. Thu .
"Genomic Changes Associated with the Evolutionary Transitions of Nostoc to a Plant Symbiont". United States. https://doi.org/10.1093/molbev/msy029.
@article{osti_1434367,
title = {Genomic Changes Associated with the Evolutionary Transitions of Nostoc to a Plant Symbiont},
author = {Warshan, Denis and Liaimer, Anton and Pederson, Eric and Kim, Sea-Yong and Shapiro, Nicole and Woyke, Tanja and Altermark, Bjørn and Pawlowski, Katharina and Weyman, Philip D. and Dupont, Christopher L. and Rasmussen, Ulla and Perna, ed., Nicole},
abstractNote = {Cyanobacteria belonging to the genus Nostoc comprise free-living strains and also facultative plant symbionts. Symbiotic strains can enter into symbiosis with taxonomically diverse range of host plants. Little is known about genomic changes associated with evolutionary transition of Nostoc from free-living to plant symbiont. Here, we compared the genomes derived from 11 symbiotic Nostoc strains isolated from different host plants and infer phylogenetic relationships between strains. Phylogenetic reconstructions of 89 Nostocales showed that symbiotic Nostoc strains with a broad host range, entering epiphytic and intracellular or extracellular endophytic interactions, form a monophyletic clade indicating a common evolutionary history. A polyphyletic origin was found for Nostoc strains which enter only extracellular symbioses, and inference of transfer events implied that this trait was likely acquired several times in the evolution of the Nostocales. Symbiotic Nostoc strains showed enriched functions in transport and metabolism of organic sulfur, chemotaxis and motility, as well as the uptake of phosphate, branched-chain amino acids, and ammonium. The genomes of the intracellular clade differ from that of other Nostoc strains, with a gain/enrichment of genes encoding proteins to generate L-methionine from sulfite and pathways for the degradation of the plant metabolites vanillin and vanillate, and of the macromolecule xylan present in plant cell walls. These compounds could function as C-sources for members of the intracellular clade. Molecular clock analysis indicated that the intracellular clade emerged ca. 600 Ma, suggesting that intracellular Nostoc symbioses predate the origin of land plants and the emergence of their extant hosts.},
doi = {10.1093/molbev/msy029},
journal = {Molecular Biology and Evolution},
number = 5,
volume = 35,
place = {United States},
year = {Thu Mar 15 00:00:00 EDT 2018},
month = {Thu Mar 15 00:00:00 EDT 2018}
}
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Cited by: 28 works
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Figures / Tables:
Table 1: Host Range of Nostoc sp. and Symbiotic Localization.
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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
Seasonal variation in nifH abundance and expression of cyanobacterial communities associated with boreal feather mosses
journal, February 2016
- Warshan, Denis; Bay, Guillaume; Nahar, Nurun
- The ISME Journal, Vol. 10, Issue 9
Mechanism of De Novo Branched-Chain Amino Acid Synthesis as an Alternative Electron Sink in Hypoxic Aspergillus nidulans Cells
journal, January 2010
- Shimizu, M.; Fujii, T.; Masuo, S.
- Applied and Environmental Microbiology, Vol. 76, Issue 5
PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments
journal, July 2006
- Suyama, M.; Torrents, D.; Bork, P.
- Nucleic Acids Research, Vol. 34, Issue Web Server
Sinorhizobium meliloti Requires a Cobalamin-Dependent Ribonucleotide Reductase for Symbiosis With Its Plant Host
journal, December 2010
- Taga, Michiko E.; Walker, Graham C.
- Molecular Plant-Microbe Interactions, Vol. 23, Issue 12
A reconstruction of Archean biological diversity based on molecular fossils from the 2.78 to 2.45 billion-year-old Mount Bruce Supergroup, Hamersley Basin, Western Australia
journal, November 2003
- Brocks, Jochen J.; Buick, Roger; Summons, Roger E.
- Geochimica et Cosmochimica Acta, Vol. 67, Issue 22
Proterozoic photosynthesis - a critical review
journal, October 2015
- Butterfield, Nicholas J.
- Palaeontology, Vol. 58, Issue 6
Nostopeptolide plays a governing role during cellular differentiation of the symbiotic cyanobacterium Nostoc punctiforme
journal, January 2015
- Liaimer, Anton; Helfrich, Eric J. N.; Hinrichs, Katrin
- Proceedings of the National Academy of Sciences, Vol. 112, Issue 6
Reconstitution of the symbiosis of Gunnera manicata Linden: cyanobacterial specificity
journal, April 1994
- Johansson, Christina; Bergman, Birgitta
- New Phytologist, Vol. 126, Issue 4
Endophytic cyanobacteria in a 400-million-yr-old land plant: A scenario for the origin of a symbiosis?
journal, January 2009
- Krings, Michael; Hass, Hagen; Kerp, Hans
- Review of Palaeobotany and Palynology, Vol. 153, Issue 1-2
Geological constraints on the origin of oxygenic photosynthesis
journal, September 2010
- Farquhar, James; Zerkle, Aubrey L.; Bekker, Andrey
- Photosynthesis Research, Vol. 107, Issue 1
Estimating the timing of early eukaryotic diversification with multigene molecular clocks
journal, August 2011
- Parfrey, L. W.; Lahr, D. J. G.; Knoll, A. H.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 33
The evolutionary diversification of cyanobacteria: Molecular-phylogenetic and paleontological perspectives
journal, March 2006
- Tomitani, A.; Knoll, A. H.; Cavanaugh, C. M.
- Proceedings of the National Academy of Sciences, Vol. 103, Issue 14
Molybdenum and phosphorus limitation of moss-associated nitrogen fixation in boreal ecosystems
journal, November 2016
- Rousk, Kathrin; Degboe, Jefferson; Michelsen, Anders
- New Phytologist, Vol. 214, Issue 1
Genomic perspectives on the birth and spread of plastids: Fig. 1.
journal, April 2015
- Archibald, John M.
- Proceedings of the National Academy of Sciences, Vol. 112, Issue 33
Sinorhizobium meliloti bluB is necessary for production of 5,6-dimethylbenzimidazole, the lower ligand of B12
journal, March 2006
- Campbell, G. R. O.; Taga, M. E.; Mistry, K.
- Proceedings of the National Academy of Sciences, Vol. 103, Issue 12
Bayes Empirical Bayes Inference of Amino Acid Sites Under Positive Selection
journal, January 2005
- Yang, Z.
- Molecular Biology and Evolution, Vol. 22, Issue 4
Lichen-Like Symbiosis 600 Million Years Ago
journal, May 2005
- Yuan, X.
- Science, Vol. 308, Issue 5724
Endosymbiotic theory for organelle origins
journal, December 2014
- Zimorski, Verena; Ku, Chuan; Martin, William F.
- Current Opinion in Microbiology, Vol. 22
Origin and diversification of living cycads: a cautionary tale on the impact of the branching process prior in Bayesian molecular dating
journal, April 2015
- Condamine, Fabien L.; Nagalingum, Nathalie S.; Marshall, Charles R.
- BMC Evolutionary Biology, Vol. 15, Issue 1
The Smallest Known Genomes of Multicellular and Toxic Cyanobacteria: Comparison, Minimal Gene Sets for Linked Traits and the Evolutionary Implications
journal, February 2010
- Stucken, Karina; John, Uwe; Cembella, Allan
- PLoS ONE, Vol. 5, Issue 2
Phylogeny and Divergence Time Estimates for the Fern Genus Azolla (Salviniaceae)
journal, September 2007
- Metzgar, Jordan S.; Schneider, Harald; Pryer, Kathleen M.
- International Journal of Plant Sciences, Vol. 168, Issue 7
The amt Gene Cluster of the Heterocyst-Forming Cyanobacterium Anabaena sp. Strain PCC 7120
journal, August 2008
- Paz-Yepes, J.; Merino-Puerto, V.; Herrero, A.
- Journal of Bacteriology, Vol. 190, Issue 19
Role of Symbiotic Auxotrophy in the Rhizobium-Legume Symbioses
journal, November 2010
- Prell, Jurgen; Bourdès, Alexandre; Kumar, Shalini
- PLoS ONE, Vol. 5, Issue 11
Characterization of the -Ketoadipate Pathway in Sinorhizobium meliloti
journal, August 2006
- MacLean, A. M.; MacPherson, G.; Aneja, P.
- Applied and Environmental Microbiology, Vol. 72, Issue 8
Phenotypic and genotypic comparison of symbiotic and free-living cyanobacteria from a single field site.
journal, January 1997
- West, N. J.; Adams, D. G.
- Applied and environmental microbiology, Vol. 63, Issue 11
The Puzzle of Plastid Evolution
journal, January 2009
- Archibald, John M.
- Current Biology, Vol. 19, Issue 2
High-throughput mapping of cell-wall polymers within and between plants using novel microarrays: Glycan microarrays for plant cell-wall analysis
journal, June 2007
- Moller, Isabel; Sørensen, Iben; Bernal, Adriana J.
- The Plant Journal, Vol. 50, Issue 6
OrthoMCL: Identification of Ortholog Groups for Eukaryotic Genomes
journal, September 2003
- Li, L.
- Genome Research, Vol. 13, Issue 9
Biological nitrogen fixation in non-legume plants
journal, March 2013
- Santi, Carole; Bogusz, Didier; Franche, Claudine
- Annals of Botany, Vol. 111, Issue 5
Extant diversity of bryophytes emerged from successive post-Mesozoic diversification bursts
journal, October 2014
- Laenen, B.; Shaw, B.; Schneider, H.
- Nature Communications, Vol. 5, Issue 1
Exploring Cyanobacterial Mutualisms
journal, December 2007
- Usher, Kayley M.; Bergman, Birgitta; Raven, John A.
- Annual Review of Ecology, Evolution, and Systematics, Vol. 38, Issue 1
A Genetic and Chemical Perspective on Symbiotic Recruitment of Cyanobacteria of the Genus Nostoc into the Host Plant Blasia pusilla L.
journal, November 2016
- Liaimer, Anton; Jensen, John B.; Dittmann, Elke
- Frontiers in Microbiology, Vol. 7
Studies on initiation and development of the partner association inGeosiphon pyriforme (K�tz.) v. Wettstein, a unique endocytobiotic system of a fungus (Glomales) and the cyanobacteriumNostoc punctiforme (K�tz.) Hariot
journal, March 1996
- Mollenhauer, D.; Mollenhauer, R.; Kluge, M.
- Protoplasma, Vol. 193, Issue 1-4
Geosiphon pyriforme , an Endosymbiotic Association of Fungus and Cyanobacteria: the Spore Structure Resembles that of Arbuscular Mycorrhizal (AM) Fungi
journal, February 1994
- Schüßler, A.; Mollenhauer, D.; Schnepf, E.
- Botanica Acta, Vol. 107, Issue 1
Phylogeny of symbiotic cyanobacteria within the genus Nostoc based on 16S rDNA sequence analyses
journal, November 2004
- Svenning, Mette M.; Eriksson, Torsten; Rasmussen, Ulla
- Archives of Microbiology, Vol. 183, Issue 1
Concerted and Birth-and-Death Evolution of Multigene Families
journal, December 2005
- Nei, Masatoshi; Rooney, Alejandro P.
- Annual Review of Genetics, Vol. 39, Issue 1
Symbiotic Nitrogen Fixation and the Challenges to Its Extension to Nonlegumes
journal, April 2016
- Mus, Florence; Crook, Matthew B.; Garcia, Kevin
- Applied and Environmental Microbiology, Vol. 82, Issue 13
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies
journal, January 2014
- Stamatakis, Alexandros
- Bioinformatics, Vol. 30, Issue 9
Feathermoss and epiphytic Nostoc cooperate differently: expanding the spectrum of plant–cyanobacteria symbiosis
journal, August 2017
- Warshan, Denis; Espinoza, Josh L.; Stuart, Rhona K.
- The ISME Journal, Vol. 11, Issue 12
Nitrogen fixation and transfer in open ocean diatom–cyanobacterial symbioses
journal, March 2011
- Foster, Rachel A.; Kuypers, Marcel M. M.; Vagner, Tomas
- The ISME Journal, Vol. 5, Issue 9
A polyketide interferes with cellular differentiation in the symbiotic cyanobacterium Nostoc punctiforme: Cellular differentiation in Nostoc punctiforme
journal, May 2011
- Liaimer, Anton; Jenke-Kodama, Holger; Ishida, Keishi
- Environmental Microbiology Reports, Vol. 3, Issue 5
Endosymbiosis and Eukaryotic Cell Evolution
journal, October 2015
- Archibald, John M.
- Current Biology, Vol. 25, Issue 19
Statistical methods for detecting molecular adaptation
journal, December 2000
- Yang, Ziheng; Bielawski, Joseph P.
- Trends in Ecology & Evolution, Vol. 15, Issue 12
Unicellular Cyanobionts in open Ocean Dinoflagellates, Radiolarians, and Tintinnids: Ultrastructural Characterization and Immuno-Localization of Phycoerythrin and Nitrogenase1
journal, April 2006
- Foster, Rachel A.; Carpenter, Edward J.; Bergman, Birgitta
- Journal of Phycology, Vol. 42, Issue 2
Boreal feather mosses secrete chemical signals to gain nitrogen
journal, June 2013
- Bay, Guillaume; Nahar, Nurun; Oubre, Matthieu
- New Phytologist, Vol. 200, Issue 1
Symbiosis between the cyanobacterium Nostoc and the liverwort Blasia requires a CheR-type MCP methyltransferase
journal, December 2012
- Duggan, Paula S.; Thiel, Teresa; Adams, David G.
- Symbiosis, Vol. 59, Issue 2
Cryptospores and cryptophytes reveal hidden diversity in early land floras
journal, January 2014
- Edwards, Dianne; Morris, Jennifer L.; Richardson, John B.
- New Phytologist, Vol. 202, Issue 1
trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses
journal, June 2009
- Capella-Gutierrez, S.; Silla-Martinez, J. M.; Gabaldon, T.
- Bioinformatics, Vol. 25, Issue 15
Count: evolutionary analysis of phylogenetic profiles with parsimony and likelihood
journal, June 2010
- Csuos, M.
- Bioinformatics, Vol. 26, Issue 15
A fast method for calculating reliable event supports in tree reconciliations via Pareto optimality
journal, November 2015
- To, Thu-Hien; Jacox, Edwin; Ranwez, Vincent
- BMC Bioinformatics, Vol. 16, Issue 1
Molecular and biotechnological aspects of xylanases
journal, July 1999
- Kulkarni, Neeta; Shendye, Abhay; Rao, Mala
- FEMS Microbiology Reviews, Vol. 23, Issue 4, p. 411-456
Phylogenetic modeling of lateral gene transfer reconstructs the pattern and relative timing of speciations
journal, October 2012
- Szollosi, G. J.; Boussau, B.; Abby, S. S.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 43
Decoding how a soil bacterium extracts building blocks and metabolic energy from ligninolysis provides road map for lignin valorization
journal, September 2016
- Varman, Arul M.; He, Lian; Follenfant, Rhiannon
- Proceedings of the National Academy of Sciences, Vol. 113, Issue 40
Cryptic carbon and sulfur cycling between surface ocean plankton
journal, December 2014
- Durham, Bryndan P.; Sharma, Shalabh; Luo, Haiwei
- Proceedings of the National Academy of Sciences, Vol. 112, Issue 2
Dating the rise of atmospheric oxygen
journal, January 2004
- Bekker, A.; Holland, H. D.; Wang, P. -L.
- Nature, Vol. 427, Issue 6970
Implications of streamlining theory for microbial ecology
journal, April 2014
- Giovannoni, Stephen J.; Cameron Thrash, J.; Temperton, Ben
- The ISME Journal, Vol. 8, Issue 8
Genetic Analysis Reveals the Identity of the Photoreceptor for Phototaxis in Hormogonium Filaments of Nostoc punctiforme
journal, December 2014
- Campbell, Elsie L.; Hagen, Kari D.; Chen, Rui
- Journal of Bacteriology, Vol. 197, Issue 4
Enzymatic deconstruction of xylan for biofuel production
journal, February 2009
- Dodd, Dylan; Cann, Isaac K. O.
- GCB Bioenergy, Vol. 1, Issue 1
The NtcA-Regulated amtB Gene Is Necessary for Full Methylammonium Uptake Activity in the Cyanobacterium Synechococcus elongatus
journal, August 2007
- Paz-Yepes, J.; Herrero, A.; Flores, E.
- Journal of Bacteriology, Vol. 189, Issue 21
Host Selection of Symbiotic Cyanobacteria in 31 Species of the Australian Cycad Genus: Macrozamia (Zamiaceae)
journal, June 2010
- Gehringer, Michelle M.; Pengelly, Jasper J. L.; Cuddy, William S.
- Molecular Plant-Microbe Interactions, Vol. 23, Issue 6
Phenolics and Plant Allelopathy
journal, December 2010
- Li, Zhao-Hui; Wang, Qiang; Ruan, Xiao
- Molecules, Vol. 15, Issue 12
BluB cannibalizes flavin to form the lower ligand of vitamin B12
journal, March 2007
- Taga, Michiko E.; Larsen, Nicholas A.; Howard-Jones, Annaleise R.
- Nature, Vol. 446, Issue 7134
Molybdenum limitation of asymbiotic nitrogen fixation in tropical forest soils
journal, December 2008
- Barron, Alexander R.; Wurzburger, Nina; Bellenger, Jean Phillipe
- Nature Geoscience, Vol. 2, Issue 1
Evaluation of an Improved Branch-Site Likelihood Method for Detecting Positive Selection at the Molecular Level
journal, August 2005
- Zhang, J.
- Molecular Biology and Evolution, Vol. 22, Issue 12
ecceTERA: comprehensive gene tree-species tree reconciliation using parsimony: Table 1.
journal, February 2016
- Jacox, Edwin; Chauve, Cedric; Szöllősi, Gergely J.
- Bioinformatics, Vol. 32, Issue 13
Characteristics of Hormogonia Formation by Symbiotic Nostoc spp. in Response to the Presence of Anthoceros punctatus or Its Extracellular Products
journal, January 1989
- Campbell, Elsie Lin; Meeks, John C.
- Applied and Environmental Microbiology, Vol. 55, Issue 1
The Number, Speed, and Impact of Plastid Endosymbioses in Eukaryotic Evolution
journal, April 2013
- Keeling, Patrick J.
- Annual Review of Plant Biology, Vol. 64, Issue 1
Hemicellulose bioconversion
journal, May 2003
- Saha, Badal C.
- Journal of Industrial Microbiology and Biotechnology, Vol. 30, Issue 5
Phylogenetic analyses of cyanobacterial genomes: Quantification of horizontal gene transfer events
journal, August 2006
- Zhaxybayeva, O.
- Genome Research, Vol. 16, Issue 9
MUSCLE: multiple sequence alignment with high accuracy and high throughput
journal, March 2004
- Edgar, R. C.
- Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797
Land plant evolutionary timeline: Gene effects are secondary to fossil constraints in relaxed clock estimation of age and substitution rates
journal, March 2013
- Magallón, Susana; Hilu, Khidir W.; Quandt, Dietmar
- American Journal of Botany, Vol. 100, Issue 3
A Comprehensive Study of Cyanobacterial Morphological and Ecological Evolutionary Dynamics through Deep Geologic Time
journal, September 2016
- Uyeda, Josef C.; Harmon, Luke J.; Blank, Carrine E.
- PLOS ONE, Vol. 11, Issue 9
Biological nitrogen fixation: rates, patterns and ecological controls in terrestrial ecosystems
journal, July 2013
- Vitousek, Peter M.; Menge, Duncan N. L.; Reed, Sasha C.
- Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 368, Issue 1621
PAML 4: Phylogenetic Analysis by Maximum Likelihood
journal, April 2007
- Yang, Z.
- Molecular Biology and Evolution, Vol. 24, Issue 8
Spores of relictual bryophytes: Diverse adaptations to life on land
journal, May 2015
- Brown, R. C.; Lemmon, B. E.; Shimamura, M.
- Review of Palaeobotany and Palynology, Vol. 216
Plastid Evolution
journal, June 2008
- Gould, Sven B.; Waller, Ross F.; McFadden, Geoffrey I.
- Annual Review of Plant Biology, Vol. 59, Issue 1
Global Gene Expression in Bradyrhizobium japonicum Cultured with Vanillin, Vanillate, 4-Hydroxybenzoate and Protocatechuate
journal, January 2006
- Ito, Naofumi; Itakura, Manabu; Eda, Shima
- Microbes and Environments, Vol. 21, Issue 4
PartitionFinder: Combined Selection of Partitioning Schemes and Substitution Models for Phylogenetic Analyses
journal, January 2012
- Lanfear, R.; Calcott, B.; Ho, S. Y. W.
- Molecular Biology and Evolution, Vol. 29, Issue 6
Genome fluctuations in cyanobacteria reflect evolutionary, developmental and adaptive traits
journal, June 2011
- Larsson, John; Nylander, Johan AA; Bergman, Birgitta
- BMC Evolutionary Biology, Vol. 11, Issue 1
Gamma Paleohexaploidy in the Stem Lineage of Core Eudicots: Significance for MADS-Box Gene and Species Diversification
journal, July 2012
- Vekemans, Dries; Proost, Sebastian; Vanneste, Kevin
- Molecular Biology and Evolution, Vol. 29, Issue 12
Cycads: evolutionary innovations and the role of plant-derived neurotoxins
journal, September 2003
- Brenner, E.
- Trends in Plant Science, Vol. 8, Issue 9
Microbiomes of Streptophyte Algae and Bryophytes Suggest That a Functional Suite of Microbiota Fostered Plant Colonization of Land
journal, June 2015
- Knack, J. J.; Wilcox, L. W.; Delaux, P. -M.
- International Journal of Plant Sciences, Vol. 176, Issue 5
VizBin - an application for reference-independent visualization and human-augmented binning of metagenomic data
journal, January 2015
- Laczny, Cedric C.; Sternal, Tomasz; Plugaru, Valentin
- Microbiome, Vol. 3, Issue 1
Tansley Review No. 116: Cyanobacterium-plant symbioses
journal, September 2000
- Rai, A. N.; SÖDerbÄCk, E.; Bergman, B.
- New Phytologist, Vol. 147, Issue 3
Unusual marine unicellular symbiosis with the nitrogen-fixing cyanobacterium UCYN-A
journal, December 2016
- Zehr, Jonathan P.; Shilova, Irina N.; Farnelid, Hanna M.
- Nature Microbiology, Vol. 2, Issue 1
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