Phylogenomics of Endogonaceae and evolution of mycorrhizas within Mucoromycota

Chang, Ying; Desirò, Alessandro; Na, Hyunsoo; Sandor, Laura; Lipzen, Anna; Clum, Alicia; Barry, Kerrie; Grigoriev, Igor V.; Martin, Francis M.; Stajich, Jason E.; Smith, Matthew E.; Bonito, Gregory; Spatafora, Joseph W.

doi:10.1111/nph.15613

Title: Phylogenomics of Endogonaceae and evolution of mycorrhizas within Mucoromycota

Journal Article · 27 November 2018 · New Phytologist

DOI: https://doi.org/10.1111/nph.15613 · OSTI ID:1580402

^[1];

^[2]; Na, Hyunsoo ^[3]; Sandor, Laura ^[3]; Lipzen, Anna ^[3]; Clum, Alicia ^[3]; Barry, Kerrie ^[3];

^[4];

^[5];

^[6];

^[7];

^[2];

^[1]

Oregon State Univ., Corvallis, OR (United States)
Michigan State Univ., East Lansing, MI (United States)
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Univ. of California, Berkeley, CA (United States)
Univ. of Lorraine, Champenoux (France). Laboratoire d'excellence ARBRE
Univ. of California, Riverside, CA (United States)
Univ. of Florida, Gainesville, FL (United States)

Endogonales (Mucoromycotina), composed of Endogonaceae and Densosporaceae, is the single known non-Dikarya order with ectomycorrhizal members. Furthermore, they form mycorrhizal-like association with some nonspermatophyte plants. It has been recently proposed that Endogonales were among the earliest mycorrhizal partners with land plants. It remains unknown whether Endogonales possess genomes with mycorrhizal-lifestyle signatures and whether Endogonales originated around the same time as land plants did. We sampled sporocarp tissue from four Endogonaceae collections and performed shotgun genome sequencing. After binning the metagenome data, we assembled and annotated the Endogonaceae genomes. We performed comparative analysis on plant-cell-wall-degrading enzymes (PCWDEs) and small secreted proteins (SSPs). We inferred phylogenetic placement of Endogonaceae and estimated the ages of Endogonaceae and Endogonales with expanded taxon sampling. Endogonaceae have large genomes with high repeat content, low diversity of PCWDEs, but without elevated SSP/secretome ratios. Dating analysis estimated that Endogonaceae originated in the Permian–Triassic boundary and Endogonales originated in the mid–late Silurian. Mycoplasma-related endobacterium sequences were identified in three Endogonaceae genomes. Endogonaceae genomes possess typical signatures of mycorrhizal lifestyle. The early origin of Endogonales suggests that the mycorrhizal association between Endogonales and plants might have played an important role during the colonization of land by plants.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: French National Research Agency; National Science Foundation (NSF); USDOE; USDOE Office of Science (SC); United States Dept. of Agriculture NIFA

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1580402

Journal Information:: New Phytologist, Journal Name: New Phytologist Journal Issue: 1 Vol. 222; ISSN 0028-646X

Publisher:: WileyCopyright Statement

Country of Publication:: United States

Language:: English

References (86)

Predicting Subcellular Localization of Proteins Based on their N-terminal Amino Acid Sequence Emanuelsson, Olof; Nielsen, Henrik; Brunak, Søren Journal of Molecular Biology, Vol. 300, Issue 4 https://doi.org/10.1006/jmbi.2000.3903	journal	July 2000
Predicting transmembrane protein topology with a hidden markov model: application to complete genomes11Edited by F. Cohen Krogh, Anders; Larsson, Björn; von Heijne, Gunnar Journal of Molecular Biology, Vol. 305, Issue 3 https://doi.org/10.1006/jmbi.2000.4315	journal	January 2001
Ectomycorrhizal Fungal Lineages: Detection of Four New Groups and Notes on Consistent Recognition of Ectomycorrhizal Taxa in High-Throughput Sequencing Studies Tedersoo, Leho; Smith, Matthew E. Biogeography of Mycorrhizal Symbiosis https://doi.org/10.1007/978-3-319-56363-3_6	book	January 2017
The Truffle Microbiome: Species and Geography Effects on Bacteria Associated with Fruiting Bodies of Hypogeous Pezizales Benucci, Gian Maria Niccolò; Bonito, Gregory M. Microbial Ecology, Vol. 72, Issue 1 https://doi.org/10.1007/s00248-016-0755-3	journal	March 2016
First detection of Endogone ectomycorrhizas in natural oak forests Yamamoto, Kohei; Endo, Naoki; Degawa, Yousuke Mycorrhiza, Vol. 27, Issue 3 https://doi.org/10.1007/s00572-016-0740-1	journal	November 2016
A new genus, Planticonsortium (Mucoromycotina), and new combination (P. tenue), for the fine root endophyte, Glomus tenue (basionym Rhizophagus tenuis) Walker, Christopher; Gollotte, Armelle; Redecker, Dirk Mycorrhiza, Vol. 28, Issue 3 https://doi.org/10.1007/s00572-017-0815-7	journal	January 2018
Morphology and phylogeny of four Endogone species and Sphaerocreas pubescens collected in Japan Yamamoto, Kohei; Degawa, Yousuke; Hirose, Dai Mycological Progress, Vol. 14, Issue 10 https://doi.org/10.1007/s11557-015-1111-6	journal	September 2015
The origin of land plants: A matter of mycotrophism Pirozynski, K. A.; Malloch, D. W. Biosystems, Vol. 6, Issue 3 https://doi.org/10.1016/0303-2647(75)90023-4	journal	March 1975
The land flora: a phototroph-fungus partnership? Selosse, M-A; Le Tacon, F. Trends in Ecology & Evolution, Vol. 13, Issue 1 https://doi.org/10.1016/S0169-5347(97)01230-5	journal	January 1998
Taxonomy, culture and mycorrhizal associations of some zygosporic Endogonaceae Warcup, J. H. Mycological Research, Vol. 94, Issue 2 https://doi.org/10.1016/S0953-7562(09)80609-6	journal	March 1990
Bioinformatics strategies for taxonomy independent binning and visualization of sequences in shotgun metagenomics Sedlar, Karel; Kupkova, Kristyna; Provaznik, Ivo Computational and Structural Biotechnology Journal, Vol. 15 https://doi.org/10.1016/j.csbj.2016.11.005	journal	January 2017
Phylogenetic analysis of the genus Modicella reveals an independent evolutionary origin of sporocarp-forming fungi in the Mortierellales Smith, Matthew E.; Gryganskyi, Andrii; Bonito, Gregory Fungal Genetics and Biology, Vol. 61 https://doi.org/10.1016/j.fgb.2013.10.001	journal	December 2013
The two-speed genomes of filamentous pathogens: waltz with plants Dong, Suomeng; Raffaele, Sylvain; Kamoun, Sophien Current Opinion in Genetics & Development, Vol. 35 https://doi.org/10.1016/j.gde.2015.09.001	journal	December 2015
Sphaerocreas pubescens is a member of the Mucoromycotina closely related to fungi associated with liverworts and hornworts Hirose, Dai; Degawa, Yousuke; Yamamoto, Kohei Mycoscience, Vol. 55, Issue 3 https://doi.org/10.1016/j.myc.2013.09.002	journal	May 2014
Reconsidering mutualistic plant–fungal interactions through the lens of effector biology Plett, Jonathan M.; Martin, Francis Current Opinion in Plant Biology, Vol. 26 https://doi.org/10.1016/j.pbi.2015.06.001	journal	August 2015
A mycorrhizal revolution Hoysted, Grace A.; Kowal, Jill; Jacob, Alison Current Opinion in Plant Biology, Vol. 44 https://doi.org/10.1016/j.pbi.2017.12.004	journal	August 2018
Symbiotic options for the conquest of land Field, Katie J.; Pressel, Silvia; Duckett, Jeffrey G. Trends in Ecology & Evolution, Vol. 30, Issue 8 https://doi.org/10.1016/j.tree.2015.05.007	journal	August 2015
Who lives in a fungus? The diversity, origins and functions of fungal endobacteria living in Mucoromycota Bonfante, Paola; Desirò, Alessandro The ISME Journal, Vol. 11, Issue 8 https://doi.org/10.1038/ismej.2017.21	journal	April 2017
Full-length transcriptome assembly from RNA-Seq data without a reference genome Grabherr, Manfred G.; Haas, Brian J.; Yassour, Moran Nature Biotechnology, Vol. 29, Issue 7 https://doi.org/10.1038/nbt.1883	journal	May 2011
Mechanisms underlying beneficial plant–fungus interactions in mycorrhizal symbiosis Bonfante, Paola; Genre, Andrea Nature Communications, Vol. 1, Issue 1 https://doi.org/10.1038/ncomms1046	journal	July 2010
Ectomycorrhizal ecology is imprinted in the genome of the dominant symbiotic fungus Cenococcum geophilum Peter, Martina; Kohler, Annegret; Ohm, Robin A. Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms12662	journal	September 2016
Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists Kohler, Annegret; Kuo, Alan; Nagy, Laszlo G. Nature Genetics, Vol. 47, Issue 4 https://doi.org/10.1038/ng.3223	journal	February 2015
Fast gapped-read alignment with Bowtie 2 Langmead, Ben; Salzberg, Steven L. Nature Methods, Vol. 9, Issue 4 https://doi.org/10.1038/nmeth.1923	journal	March 2012
jModelTest 2: more models, new heuristics and parallel computing Darriba, Diego; Taboada, Guillermo L.; Doallo, Ramón Nature Methods, Vol. 9, Issue 8 https://doi.org/10.1038/nmeth.2109	journal	July 2012
Fast and sensitive protein alignment using DIAMOND Buchfink, Benjamin; Xie, Chao; Huson, Daniel H. Nature Methods, Vol. 12, Issue 1 https://doi.org/10.1038/nmeth.3176	journal	November 2014
MetaPhlAn2 for enhanced metagenomic taxonomic profiling Truong, Duy Tin; Franzosa, Eric A.; Tickle, Timothy L. Nature Methods, Vol. 12, Issue 10 https://doi.org/10.1038/nmeth.3589	journal	September 2015
Unearthing the roots of ectomycorrhizal symbioses Martin, Francis; Kohler, Annegret; Murat, Claude Nature Reviews Microbiology, Vol. 14, Issue 12 https://doi.org/10.1038/nrmicro.2016.149	journal	October 2016
Mycoplasma-related endobacteria within Mortierellomycotina fungi: diversity, distribution and functional insights into their lifestyle Desirò, Alessandro; Hao, Zhen; Liber, Julian A. The ISME Journal, Vol. 12, Issue 7 https://doi.org/10.1038/s41396-018-0053-9	journal	February 2018
Evaluation of single-cell genomics to address evolutionary questions using three SAGs of the choanoflagellate Monosiga brevicollis López-Escardó, David; Grau-Bové, Xavier; Guillaumet-Adkins, Amy Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-11466-9	journal	September 2017
Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis Tisserant, E.; Malbreil, M.; Kuo, A. Proceedings of the National Academy of Sciences, Vol. 110, Issue 50 https://doi.org/10.1073/pnas.1313452110	journal	November 2013
Mosaic genome of endobacteria in arbuscular mycorrhizal fungi: Transkingdom gene transfer in an ancient mycoplasma-fungus association Torres-Cortés, Gloria; Ghignone, Stefano; Bonfante, Paola Proceedings of the National Academy of Sciences, Vol. 112, Issue 25 https://doi.org/10.1073/pnas.1501540112	journal	May 2015
Minimal genomes of mycoplasma-related endobacteria are plastic and contain host-derived genes for sustained life within Glomeromycota Naito, Mizue; Morton, Joseph B.; Pawlowska, Teresa E. Proceedings of the National Academy of Sciences, Vol. 112, Issue 25 https://doi.org/10.1073/pnas.1501676112	journal	May 2015
Bifiguratus adelaidae , gen. et sp. nov., a new member of Mucoromycotina in endophytic and soil-dwelling habitats Torres-Cruz, Terry J.; Billingsley Tobias, Terri L.; Almatruk, Maryam Mycologia, Vol. 109, Issue 3 https://doi.org/10.1080/00275514.2017.1364958	journal	May 2017
How Many Bootstrap Replicates Are Necessary? Pattengale, Nicholas D.; Alipour, Masoud; Bininda-Emonds, Olaf R. P. Journal of Computational Biology, Vol. 17, Issue 3 https://doi.org/10.1089/cmb.2009.0179	journal	March 2010
SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing Bankevich, Anton; Nurk, Sergey; Antipov, Dmitry Journal of Computational Biology, Vol. 19, Issue 5 https://doi.org/10.1089/cmb.2012.0021	journal	May 2012
r8s: inferring absolute rates of molecular evolution and divergence times in the absence of a molecular clock Sanderson, M. J. Bioinformatics, Vol. 19, Issue 2 https://doi.org/10.1093/bioinformatics/19.2.301	journal	January 2003
De novo identification of repeat families in large genomes Price, A. L.; Jones, N. C.; Pevzner, P. A. Bioinformatics, Vol. 21, Issue Suppl 1 https://doi.org/10.1093/bioinformatics/bti1018	journal	June 2005
trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses Capella-Gutierrez, S.; Silla-Martinez, J. M.; Gabaldon, T. Bioinformatics, Vol. 25, Issue 15 https://doi.org/10.1093/bioinformatics/btp348	journal	June 2009
Search and clustering orders of magnitude faster than BLAST Edgar, Robert C. Bioinformatics, Vol. 26, Issue 19, p. 2460-2461 https://doi.org/10.1093/bioinformatics/btq461	journal	August 2010
Inferring duplications, losses, transfers and incomplete lineage sorting with nonbinary species trees Stolzer, Maureen; Lai, Han; Xu, Minli Bioinformatics, Vol. 28, Issue 18 https://doi.org/10.1093/bioinformatics/bts386	journal	September 2012
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies Stamatakis, Alexandros Bioinformatics, Vol. 30, Issue 9 https://doi.org/10.1093/bioinformatics/btu033	journal	January 2014
BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs Simão, Felipe A.; Waterhouse, Robert M.; Ioannidis, Panagiotis Bioinformatics, Vol. 31, Issue 19 https://doi.org/10.1093/bioinformatics/btv351	journal	June 2015
Ultra-low input transcriptomics reveal the spore functional content and phylogenetic affiliations of poorly studied arbuscular mycorrhizal fungi Beaudet, Denis; Chen, Eric C. H.; Mathieu, Stephanie DNA Research, Vol. 25, Issue 2 https://doi.org/10.1093/dnares/dsx051	journal	December 2017
Phylogenomic Analyses Indicate that Early Fungi Evolved Digesting Cell Walls of Algal Ancestors of Land Plants Chang, Ying; Wang, Sishuo; Sekimoto, Satoshi Genome Biology and Evolution, Vol. 7, Issue 6 https://doi.org/10.1093/gbe/evv090	journal	May 2015
MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability Katoh, K.; Standley, D. M. Molecular Biology and Evolution, Vol. 30, Issue 4 https://doi.org/10.1093/molbev/mst010	journal	January 2013
UniProt: the Universal Protein knowledgebase Apweiler, R. Nucleic Acids Research, Vol. 32, Issue 90001 https://doi.org/10.1093/nar/gkh131	journal	January 2004
WoLF PSORT: protein localization predictor Horton, P.; Park, K. -J.; Obayashi, T. Nucleic Acids Research, Vol. 35, Issue Web Server https://doi.org/10.1093/nar/gkm259	journal	May 2007
dbCAN: a web resource for automated carbohydrate-active enzyme annotation Yin, Yanbin; Mao, Xizeng; Yang, Jincai Nucleic Acids Research, Vol. 40, Issue W1 https://doi.org/10.1093/nar/gks479	journal	May 2012
PATRIC, the bacterial bioinformatics database and analysis resource Wattam, Alice R.; Abraham, David; Dalay, Oral Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1099	journal	November 2013
Selection of Conserved Blocks from Multiple Alignments for Their Use in Phylogenetic Analysis Castresana, J. Molecular Biology and Evolution, Vol. 17, Issue 4 https://doi.org/10.1093/oxfordjournals.molbev.a026334	journal	April 2000
MrBayes 3.2: Efficient Bayesian Phylogenetic Inference and Model Choice Across a Large Model Space Ronquist, Fredrik; Teslenko, Maxim; van der Mark, Paul Systematic Biology, Vol. 61, Issue 3 https://doi.org/10.1093/sysbio/sys029	journal	February 2012
The dawn of symbiosis between plants and fungi Bidartondo, Martin I.; Read, David J.; Trappe, James M. Biology Letters, Vol. 7, Issue 4 https://doi.org/10.1098/rsbl.2010.1203	journal	February 2011
Fungal symbioses in hornworts: a chequered history Desirò, Alessandro; Duckett, Jeffrey G.; Pressel, Silvia Proceedings of the Royal Society B: Biological Sciences, Vol. 280, Issue 1759 https://doi.org/10.1098/rspb.2013.0207	journal	May 2013
‘Candidatus Moeniiplasma glomeromycotorum’, an endobacterium of arbuscular mycorrhizal fungi Naito, Mizue; Desirò, Alessandro; González, Jonathan B. International Journal of Systematic and Evolutionary Microbiology, Vol. 67, Issue 5, p. 1177-1184 https://doi.org/10.1099/ijsem.0.001785	journal	May 2017
MAKER: An easy-to-use annotation pipeline designed for emerging model organism genomes Cantarel, B. L.; Korf, I.; Robb, S. M. C. Genome Research, Vol. 18, Issue 1 https://doi.org/10.1101/gr.6743907	journal	November 2007
The Origin and Early Evolution of Roots Kenrick, P.; Strullu-Derrien, C. PLANT PHYSIOLOGY, Vol. 166, Issue 2 https://doi.org/10.1104/pp.114.244517	journal	September 2014
Black truffle - associated bacterial communities during the development and maturation of T uber melanosporum ascocarps and putative functional roles Antony-Babu, Sanjay; Deveau, Aurélie; Van Nostrand, Joy D. Environmental Microbiology, Vol. 16, Issue 9 https://doi.org/10.1111/1462-2920.12294	journal	November 2013
Metagenome sequence of E laphomyces granulatus from sporocarp tissue reveals Ascomycota ectomycorrhizal fingerprints of genome expansion and a Proteobacteria -rich microbiome Quandt, C. Alisha; Kohler, Annegret; Hesse, Cedar N. Environmental Microbiology, Vol. 17, Issue 8 https://doi.org/10.1111/1462-2920.12840	journal	April 2015
New Phytologist ? an evolving host for mycorrhizal research Martin, Francis; Slater, Holly New Phytologist, Vol. 174, Issue 2 https://doi.org/10.1111/j.1469-8137.2007.02058.x	journal	April 2007
Evolutionary Stability in a 400-Million-Year-Old Heritable Facultative Mutualism: Evolution in Glomeromycota-Glomeribacter Symbiosis Mondo, Stephen J.; Toomer, Kevin H.; Morton, Joseph B. Evolution, Vol. 66, Issue 8 https://doi.org/10.1111/j.1558-5646.2012.01611.x	journal	March 2012
Fungal associations in Horneophyton ligneri from the Rhynie Chert ( c . 407 million year old) closely resemble those in extant lower land plants: novel insights into ancestral plant-fungus symbioses Strullu-Derrien, Christine; Kenrick, Paul; Pressel, Silvia New Phytologist, Vol. 203, Issue 3 https://doi.org/10.1111/nph.12805	journal	April 2014
First evidence of mutualism between ancient plant lineages (Haplomitriopsida liverworts) and Mucoromycotina fungi and its response to simulated Palaeozoic changes in atmospheric CO ₂ Field, Katie J.; Rimington, William R.; Bidartondo, Martin I. New Phytologist, Vol. 205, Issue 2 https://doi.org/10.1111/nph.13024	journal	September 2014
Endogone , one of the oldest plant-associated fungi, host unique Mollicutes-related endobacteria Desirò, Alessandro; Faccio, Antonella; Kaech, Andres New Phytologist, Vol. 205, Issue 4 https://doi.org/10.1111/nph.13136	journal	October 2014
Fungal associations of basal vascular plants: reopening a closed book? Rimington, William R.; Pressel, Silvia; Duckett, Jeffrey G. New Phytologist, Vol. 205, Issue 4 https://doi.org/10.1111/nph.13221	journal	December 2014
Mycorrhizal ecology and evolution: the past, the present, and the future van der Heijden, Marcel G. A.; Martin, Francis M.; Selosse, Marc-André New Phytologist, Vol. 205, Issue 4 https://doi.org/10.1111/nph.13288	journal	February 2015
Fine endophytes ( Glomus tenue ) are related to Mucoromycotina, not Glomeromycota Orchard, Suzanne; Hilton, Sally; Bending, Gary D. New Phytologist, Vol. 213, Issue 2 https://doi.org/10.1111/nph.14268	journal	October 2016
Evolutionary history of mycorrhizal symbioses and global host plant diversity Brundrett, Mark C.; Tedersoo, Leho New Phytologist, Vol. 220, Issue 4 https://doi.org/10.1111/nph.14976	journal	January 2018
The origin and evolution of mycorrhizal symbioses: from palaeomycology to phylogenomics Strullu-Derrien, Christine; Selosse, Marc-André; Kenrick, Paul New Phytologist, Vol. 220, Issue 4 https://doi.org/10.1111/nph.15076	journal	March 2018
Ancestral alliances: Plant mutualistic symbioses with fungi and bacteria Martin, Francis M.; Uroz, Stéphane; Barker, David G. Science, Vol. 356, Issue 6340 https://doi.org/10.1126/science.aad4501	journal	May 2017
Bacterial Endosymbionts: Master Modulators of Fungal Phenotypes Araldi-Brondolo, Sarah J.; Spraker, Joseph; Shaffer, Justin P. Microbiology Spectrum, Vol. 5, Issue 5 https://doi.org/10.1128/microbiolspec.FUNK-0056-2016	journal	October 2017
Endogone pisiformis : axenic culture and associations with Sphagnum, Pinus sylvestris, Allium cepa , and Allium porrum Berch, S. M.; Fortin, J. A. Canadian Journal of Botany, Vol. 61, Issue 3 https://doi.org/10.1139/b83-100	journal	March 1983
MAKER2: an annotation pipeline and genome-database management tool for second-generation genome projects Holt, Carson; Yandell, Mark BMC Bioinformatics, Vol. 12, Issue 1 https://doi.org/10.1186/1471-2105-12-491	journal	December 2011
LTRharvest, an efficient and flexible software for de novo detection of LTR retrotransposons Ellinghaus, David; Kurtz, Stefan; Willhoeft, Ute BMC Bioinformatics, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2105-9-18	journal	January 2008
The diversity of fungal genome Mohanta, Tapan Kumar; Bae, Hanhong Biological Procedures Online, Vol. 17, Issue 1 https://doi.org/10.1186/s12575-015-0020-z	journal	April 2015
Repbase Update, a database of repetitive elements in eukaryotic genomes Bao, Weidong; Kojima, Kenji K.; Kohany, Oleksiy Mobile DNA, Vol. 6, Issue 1 https://doi.org/10.1186/s13100-015-0041-9	journal	June 2015
VizBin - an application for reference-independent visualization and human-augmented binning of metagenomic data Laczny, Cedric C.; Sternal, Tomasz; Plugaru, Valentin Microbiome, Vol. 3, Issue 1 https://doi.org/10.1186/s40168-014-0066-1	journal	January 2015
Accelerated Profile HMM Searches Eddy, Sean R. PLoS Computational Biology, Vol. 7, Issue 10 https://doi.org/10.1371/journal.pcbi.1002195	journal	October 2011
BEAST 2: A Software Platform for Bayesian Evolutionary Analysis Bouckaert, Remco; Heled, Joseph; Kühnert, Denise PLoS Computational Biology, Vol. 10, Issue 4 https://doi.org/10.1371/journal.pcbi.1003537	journal	April 2014
Comparative Analysis of Secretomes from Ectomycorrhizal Fungi with an Emphasis on Small-Secreted Proteins Pellegrin, Clement; Morin, Emmanuelle; Martin, Francis M. Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.01278	journal	November 2015
Fungi Contribute Critical but Spatially Varying Roles in Nitrogen and Carbon Cycling in Acid Mine Drainage Mosier, Annika C.; Miller, Christopher S.; Frischkorn, Kyle R. Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.00238	journal	March 2016
Kingdom-Wide Analysis of Fungal Small Secreted Proteins (SSPs) Reveals their Potential Role in Host Association Kim, Ki-Tae; Jeon, Jongbum; Choi, Jaeyoung Frontiers in Plant Science, Vol. 7 https://doi.org/10.3389/fpls.2016.00186	journal	February 2016
Fossil fungi with suggested affinities to the Endogonaceae from the Middle Triassic of Antarctica Krings, M.; Taylor, T. N.; Dotzler, N. Mycologia, Vol. 104, Issue 4 https://doi.org/10.3852/11-384	journal	March 2012
A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data Spatafora, Joseph W.; Chang, Ying; Benny, Gerald L. Mycologia, Vol. 108, Issue 5 https://doi.org/10.3852/16-042	journal	September 2016
Dating divergences in the Fungal Tree of Life: review and new analyses Taylor, J. W.; Berbee, M. L. Mycologia, Vol. 98, Issue 6 https://doi.org/10.3852/mycologia.98.6.838	journal	November 2006
Multigene phylogeny of Endogonales, an early diverging lineage offungi associated with plants Desirò, Alessandro; Rimington, William R.; Jacob, Alison IMA Fungus, Vol. 8, Issue 2 https://doi.org/10.5598/imafungus.2017.08.02.03	journal	October 2017
The genome of an intranuclear parasite, Paramicrosporidium saccamoebae, reveals alternative adaptations to obligate intracellular parasitism Quandt, C. Alisha; Beaudet, Denis; Corsaro, Daniele eLife, Vol. 6 https://doi.org/10.7554/eLife.29594	journal	November 2017

Similar Records

Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists

Journal Article · 2015 · Nature Genetics · OSTI ID:1242700

Kohler, Annegret; Kuo, Alan; Nagy, Laszlo G.; +49 more

Expanding genomics of mycorrhizal symbiosis

Journal Article · 2014 · Frontiers in Microbiology · OSTI ID:1213050

Kuo, Alan; Kohler, Annegret; Martin, Francis M.; +1 more

Comparative analysis of secretomes from Ectomycorrhizal fungi with an emphasis on small-secreted proteins

Journal Article · 2015 · Frontiers in Microbiology · OSTI ID:1241128

Pellegrin, Clement; Morin, Emmanuelle; Martin, Francis M.; +1 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Endogonaceae
Endogonales
Mucoromycota
Mycoplasma‐related endobacteria (MRE)
ectomycorrhiza
mycorrhizal
plant‐cell‐wall‐degrading enzymes

Title: Phylogenomics of Endogonaceae and evolution of mycorrhizas within Mucoromycota

Citation Formats

References (86)

Similar Records

Related Subjects