High intraspecific genome diversity in the model arbuscular mycorrhizal symbiont Rhizophagus irregularis

Chen, Eric C.  H.; Morin, Emmanuelle; Beaudet, Denis; Noel, Jessica; Yildirir, Gokalp; Ndikumana, Steve; Charron, Philippe; St-Onge, Camille; Giorgi, John; Krüger, Manuela; Marton, Timea; Ropars, Jeanne; Grigoriev, Igor V.; Hainaut, Matthieu; Henrissat, Bernard; Roux, Christophe; Martin, Francis; Corradi, Nicolas

doi:10.1111/nph.14989

High intraspecific genome diversity in the model arbuscular mycorrhizal symbiont Rhizophagus irregularis

Journal Article · Mon Jan 22 00:00:00 EST 2018 · New Phytologist

DOI:https://doi.org/10.1111/nph.14989· OSTI ID:1543996

^[1]; Morin, Emmanuelle ^[2]; Beaudet, Denis ^[1]; Noel, Jessica ^[1]; Yildirir, Gokalp ^[1]; Ndikumana, Steve ^[1]; Charron, Philippe ^[1]; St-Onge, Camille ^[1]; Giorgi, John ^[1]; Krüger, Manuela ^[1]; Marton, Timea ^[1]; Ropars, Jeanne ^[1]; Grigoriev, Igor V. ^[3]; Hainaut, Matthieu ^[4]; Henrissat, Bernard ^[5]; Roux, Christophe ^[6]; ^[2]; Corradi, Nicolas ^[1]

Univ. of Ottawa, Ottawa, ON (Canada)
Inst. National de la Recherche Agronomique (INRA), Champenoux (France)
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
Aix-Marseille Univ., Marseille (France); Inst. National de la Recherche Agronomique (INRA), Marseille (France)
Aix-Marseille Univ., Marseille (France); Inst. National de la Recherche Agronomique (INRA), Marseille (France); King Abdulaziz Univ., Jeddah (Saudi Arabia)
Univ. de Toulouse, Castanet-Tolosan (France)

Arbuscular mycorrhizal fungi (AMF) are known to improve plant fitness through the establishment of mycorrhizal symbioses. Genetic and phenotypic variations among closely related AMF isolates can significantly affect plant growth, but the genomic changes underlying this variability are unclear. To address this issue, we improved the genome assembly and gene annotation of the model strain Rhizophagus irregularis DAOM197198, and compared its gene content with five isolates of R. irregularis sampled in the same field. All isolates harbor striking genome variations, with large numbers of isolate-specific genes, gene family expansions, and evidence of interisolate genetic exchange. The observed variability affects all gene ontology terms and PFAM protein domains, as well as putative mycorrhiza-induced small secreted effector-like proteins and other symbiosis differentially expressed genes. High variability is also found in active transposable elements. Overall, these findings indicate a substantial divergence in the functioning capacity of isolates harvested from the same field, and thus their genetic potential for adaptation to biotic and abiotic changes. Our data also provide a first glimpse into the genome diversity that resides within natural populations of these symbionts, and open avenues for future analyses of plant–AMF interactions that link AMF genome variation with plant phenotype and fitness.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC); Univ. of California, Oakland, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1543996

Alternate ID(s):: OSTI ID: 1481337

Journal Information:: New Phytologist, Journal Name: New Phytologist Journal Issue: 4 Vol. 220; ISSN 0028-646X

Publisher:: WileyCopyright Statement

Country of Publication:: United States

Language:: English

References (73)

Transposable elements: powerful facilitators of evolution Oliver, Keith R.; Greene, Wayne K. BioEssays, Vol. 31, Issue 7 https://doi.org/10.1002/bies.200800219	journal	July 2009
Sex or no sex: Evolutionary adaptation occurs regardless: Insights & Perspectives Seidl, Michael F.; Thomma, Bart P. H. J. BioEssays, Vol. 36, Issue 4 https://doi.org/10.1002/bies.201300155	journal	February 2014
Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis Brundrett, Mark C. Plant and Soil, Vol. 320, Issue 1-2 https://doi.org/10.1007/s11104-008-9877-9	journal	February 2009
SMURF: Genomic mapping of fungal secondary metabolite clusters Khaldi, Nora; Seifuddin, Fayaz T.; Turner, Geoff Fungal Genetics and Biology, Vol. 47, Issue 9 https://doi.org/10.1016/j.fgb.2010.06.003	journal	September 2010
Searching for clues of sexual reproduction in the genomes of arbuscular mycorrhizal fungi Riley, Rohan; Corradi, Nicolas Fungal Ecology, Vol. 6, Issue 1 https://doi.org/10.1016/j.funeco.2012.01.010	journal	February 2013
Uniting species- and community-oriented approaches to understand arbuscular mycorrhizal fungal diversity Öpik, Maarja; Davison, John Fungal Ecology, Vol. 24 https://doi.org/10.1016/j.funeco.2016.07.005	journal	December 2016
Fungal Mating in the Most Widespread Plant Symbionts? Corradi, Nicolas; Brachmann, Andreas Trends in Plant Science, Vol. 22, Issue 2 https://doi.org/10.1016/j.tplants.2016.10.010	journal	February 2017
No sex please, we're fungi: Evolutionary genetics Sanders, Ian R. Nature, Vol. 399, Issue 6738 https://doi.org/10.1038/21544	journal	June 1999
Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity van der Heijden, Marcel G. A.; Klironomos, John N.; Ursic, Margot Nature, Vol. 396, Issue 6706 https://doi.org/10.1038/23932	journal	November 1998
Population genomics reveals that within-fungus polymorphism is common and maintained in populations of the mycorrhizal fungus Rhizophagus irregularis Wyss, Tania; Masclaux, Frédéric G.; Rosikiewicz, Pawel The ISME Journal, Vol. 10, Issue 10 https://doi.org/10.1038/ismej.2016.29	journal	March 2016
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
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
Evidence for the sexual origin of heterokaryosis in arbuscular mycorrhizal fungi Ropars, Jeanne; Toro, Kinga Sędzielewska; Noel, Jessica Nature Microbiology, Vol. 1, Issue 6 https://doi.org/10.1038/nmicrobiol.2016.33	journal	March 2016
Statistical tests of selective neutrality in the age of genomics Nielsen, Rasmus Heredity, Vol. 86, Issue 6 https://doi.org/10.1046/j.1365-2540.2001.00895.x	journal	June 2001
High genetic variability and low local diversity in a population of arbuscular mycorrhizal fungi Koch, A. M.; Kuhn, G.; Fontanillas, P. Proceedings of the National Academy of Sciences, Vol. 101, Issue 8 https://doi.org/10.1073/pnas.0306441101	journal	February 2004
Genome sequencing and comparative analysis of Saccharomyces cerevisiae strain YJM789 Wei, W.; McCusker, J. H.; Hyman, R. W. Proceedings of the National Academy of Sciences, Vol. 104, Issue 31 https://doi.org/10.1073/pnas.0701291104	journal	July 2007
High-quality draft assemblies of mammalian genomes from massively parallel sequence data Gnerre, S.; MacCallum, I.; Przybylski, D. Proceedings of the National Academy of Sciences, Vol. 108, Issue 4 https://doi.org/10.1073/pnas.1017351108	journal	December 2010
Instability of repetitive DNA sequences: The role of replication in multiple mechanisms Bzymek, M.; Lovett, S. T. Proceedings of the National Academy of Sciences, Vol. 98, Issue 15 https://doi.org/10.1073/pnas.111008398	journal	July 2001
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
Improvement of Phylogenies after Removing Divergent and Ambiguously Aligned Blocks from Protein Sequence Alignments Talavera, Gerard; Castresana, Jose Systematic Biology, Vol. 56, Issue 4 https://doi.org/10.1080/10635150701472164	journal	August 2007
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
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
CEGMA: a pipeline to accurately annotate core genes in eukaryotic genomes Parra, G.; Bradnam, K.; Korf, I. Bioinformatics, Vol. 23, Issue 9 https://doi.org/10.1093/bioinformatics/btm071	journal	March 2007
Scaffolding pre-assembled contigs using SSPACE Boetzer, Marten; Henkel, Christiaan V.; Jansen, Hans J. Bioinformatics, Vol. 27, Issue 4 https://doi.org/10.1093/bioinformatics/btq683	journal	December 2010
Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data Kearse, M.; Moir, R.; Wilson, A. Bioinformatics, Vol. 28, Issue 12 https://doi.org/10.1093/bioinformatics/bts199	journal	April 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
FunGAP: Fungal Genome Annotation Pipeline using evidence-based gene model evaluation Min, Byoungnam; Grigoriev, Igor V.; Choi, In-Geol Bioinformatics, Vol. 33, Issue 18 https://doi.org/10.1093/bioinformatics/btx353	journal	June 2017
Conserved Meiotic Machinery in Glomus spp., a Putatively Ancient Asexual Fungal Lineage Halary, Sébastien; Malik, Shehre-Banoo; Lildhar, Levannia Genome Biology and Evolution, Vol. 3 https://doi.org/10.1093/gbe/evr089	journal	January 2011
Evolution of Paralogous Genes: Reconstruction of Genome Rearrangements Through Comparison of Multiple Genomes Within Staphylococcus aureus Tsuru, T. Molecular Biology and Evolution, Vol. 23, Issue 6 https://doi.org/10.1093/molbev/msk013	journal	March 2006
The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics Cantarel, B. L.; Coutinho, P. M.; Rancurel, C. Nucleic Acids Research, Vol. 37, Issue Database https://doi.org/10.1093/nar/gkn663	journal	January 2009
The genome portal of the Department of Energy Joint Genome Institute: 2014 updates Nordberg, Henrik; Cantor, Michael; Dusheyko, Serge Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1069	journal	November 2013
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
MycoCosm portal: gearing up for 1000 fungal genomes Grigoriev, Igor V.; Nikitin, Roman; Haridas, Sajeet Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1183	journal	December 2013
The Pfam protein families database: towards a more sustainable future Finn, Robert D.; Coggill, Penelope; Eberhardt, Ruth Y. Nucleic Acids Research, Vol. 44, Issue D1 https://doi.org/10.1093/nar/gkv1344	journal	December 2015
Intraspecies Interaction of Fusarium graminearum Contributes to Reduced Toxin Production and Virulence Walkowiak, Sean; Bonner, Christopher T.; Wang, Li Molecular Plant-Microbe Interactions, Vol. 28, Issue 11 https://doi.org/10.1094/MPMI-06-15-0120-R	journal	November 2015
Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks Shannon, P. Genome Research, Vol. 13, Issue 11 https://doi.org/10.1101/gr.1239303	journal	November 2003
Transposons passively and actively contribute to evolution of the two-speed genome of a fungal pathogen Faino, Luigi; Seidl, Michael F.; Shi-Kunne, Xiaoqian Genome Research, Vol. 26, Issue 8 https://doi.org/10.1101/gr.204974.116	journal	June 2016
The Bioperl Toolkit: Perl Modules for the Life Sciences Stajich, J. E. Genome Research, Vol. 12, Issue 10 https://doi.org/10.1101/gr.361602	journal	October 2002
Automated De Novo Identification of Repeat Sequence Families in Sequenced Genomes Bao, Z. Genome Research, Vol. 12, Issue 8 https://doi.org/10.1101/gr.88502	journal	July 2002
Genetic variability in a population of arbuscular mycorrhizal fungi causes variation in plant growth: Functional variability in AMF populations Koch, Alexander M.; Croll, Daniel; Sanders, Ian R. Ecology Letters, Vol. 9, Issue 2 https://doi.org/10.1111/j.1461-0248.2005.00853.x	journal	November 2005
Genetic diversity and host plant preferences revealed by simple sequence repeat and mitochondrial markers in a population of the arbuscular mycorrhizal fungus Glomus intraradices Croll, Daniel; Wille, Lukas; Gamper, Hannes A. New Phytologist, Vol. 178, Issue 3 https://doi.org/10.1111/j.1469-8137.2008.02381.x	journal	May 2008
‘ Glomus intraradices DAOM197198’, a model fungus in arbuscular mycorrhiza research, is not Glomus intraradices Stockinger, Herbert; Walker, Christopher; Schüßler, Arthur New Phytologist, Vol. 183, Issue 4 https://doi.org/10.1111/j.1469-8137.2009.02874.x	journal	September 2009
Molecular trait indicators: moving beyond phylogeny in arbuscular mycorrhizal ecology Gamper, Hannes A.; Van Der Heijden, Marcel G. A.; Kowalchuk, George A. New Phytologist, Vol. 185, Issue 1 https://doi.org/10.1111/j.1469-8137.2009.03058.x	journal	October 2009
Significant genetic and phenotypic changes arising from clonal growth of a single spore of an arbuscular mycorrhizal fungus over multiple generations Ehinger, Martine O.; Croll, Daniel; Koch, Alexander M. New Phytologist, Vol. 196, Issue 3 https://doi.org/10.1111/j.1469-8137.2012.04278.x	journal	August 2012
Comparative genome analysis of a Saccharomyces cerevisiae wine strain Borneman, Anthony; Forgan, Angus; Pretorius, Isak FEMS Yeast Research, Vol. 8, Issue 7, p. 1185-1195 https://doi.org/10.1111/j.1567-1364.2008.00434.x	journal	November 2008
Towards a unified paradigm for sequence-based identification of fungi Kõljalg, Urmas; Nilsson, R. Henrik; Abarenkov, Kessy Molecular Ecology, Vol. 22, Issue 21 https://doi.org/10.1111/mec.12481	journal	September 2013
Evolution, selection and isolation: a genomic view of speciation in fungal plant pathogens Stukenbrock, Eva Holtgrewe New Phytologist, Vol. 199, Issue 4 https://doi.org/10.1111/nph.12374	journal	June 2013
Extreme diversification of the mating type - high-mobility group ( MATA - HMG ) gene family in a plant-associated arbuscular mycorrhizal fungus Riley, Rohan; Charron, Philippe; Idnurm, Alexander New Phytologist, Vol. 201, Issue 1 https://doi.org/10.1111/nph.12462	journal	August 2013
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
Biology and evolution of arbuscular mycorrhizal symbiosis in the light of genomics Kamel, Laurent; Keller-Pearson, Michelle; Roux, Christophe New Phytologist, Vol. 213, Issue 2 https://doi.org/10.1111/nph.14263	journal	October 2016
Arbuscular mycorrhiza-specific enzymes FatM and RAM2 fine-tune lipid biosynthesis to promote development of arbuscular mycorrhiza Bravo, Armando; Brands, Mathias; Wewer, Vera New Phytologist, Vol. 214, Issue 4 https://doi.org/10.1111/nph.14533	journal	April 2017
Glomeromycotina: what is a species and why should we care? Bruns, Thomas D.; Corradi, Nicolas; Redecker, Dirk New Phytologist, Vol. 220, Issue 4 https://doi.org/10.1111/nph.14913	journal	November 2017
Transposable Elements, Epigenetics, and Genome Evolution Fedoroff, N. V. Science, Vol. 338, Issue 6108 https://doi.org/10.1126/science.338.6108.758	journal	November 2012
Global assessment of arbuscular mycorrhizal fungus diversity reveals very low endemism Davison, J.; Moora, M.; Opik, M. Science, Vol. 349, Issue 6251 https://doi.org/10.1126/science.aab1161	journal	August 2015
Comment on "Global assessment of arbuscular mycorrhizal fungus diversity reveals very low endemism" Bruns, T. D.; Taylor, J. W. Science, Vol. 351, Issue 6275 https://doi.org/10.1126/science.aad4228	journal	February 2016
Gene Copy Number Polymorphisms in an Arbuscular Mycorrhizal Fungal Population Corradi, N.; Croll, D.; Colard, A. Applied and Environmental Microbiology, Vol. 73, Issue 1 https://doi.org/10.1128/AEM.01574-06	journal	November 2006
Genomic Plasticity of the Human Fungal Pathogen Candida albicans Selmecki, Anna; Forche, Anja; Berman, Judith Eukaryotic Cell, Vol. 9, Issue 7 https://doi.org/10.1128/EC.00060-10	journal	May 2010
The Evolution of Orphan Regions in Genomes of a Fungal Pathogen of Wheat Plissonneau, Clémence; Stürchler, Alessandra; Croll, Daniel mBio, Vol. 7, Issue 5 https://doi.org/10.1128/mBio.01231-16	journal	October 2016
Arbuscular Mycorrhiza: The Challenge to Understand the Genetics of the Fungal Partner Sanders, Ian R.; Croll, Daniel Annual Review of Genetics, Vol. 44, Issue 1 https://doi.org/10.1146/annurev-genet-102108-134239	journal	December 2010
Plants, Mycorrhizal Fungi, and Bacteria: A Network of Interactions Bonfante, Paola; Anca, Iulia-Andra Annual Review of Microbiology, Vol. 63, Issue 1 https://doi.org/10.1146/annurev.micro.091208.073504	journal	October 2009
EGN: a wizard for construction of gene and genome similarity networks Halary, Sébastien; McInerney, James O.; Lopez, Philippe BMC Evolutionary Biology, Vol. 13, Issue 1 https://doi.org/10.1186/1471-2148-13-146	journal	January 2013
Recombination in Glomus intraradices, a supposed ancient asexual arbuscular mycorrhizal fungus Croll, Daniel; Sanders, Ian R. BMC Evolutionary Biology, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2148-9-13	journal	January 2009
Environmental change drives accelerated adaptation through stimulated copy number variation Hull, Ryan M.; Cruz, Cristina; Jack, Carmen V. PLOS Biology, Vol. 15, Issue 6 https://doi.org/10.1371/journal.pbio.2001333	journal	June 2017
Finished Genome of the Fungal Wheat Pathogen Mycosphaerella graminicola Reveals Dispensome Structure, Chromosome Plasticity, and Stealth Pathogenesis Goodwin, Stephen B.; Ben M'Barek, Sarrah; Dhillon, Braham PLoS Genetics, Vol. 7, Issue 6 https://doi.org/10.1371/journal.pgen.1002070	journal	June 2011
Single Nucleus Genome Sequencing Reveals High Similarity among Nuclei of an Endomycorrhizal Fungus Lin, Kui; Limpens, Erik; Zhang, Zhonghua PLoS Genetics, Vol. 10, Issue 1 https://doi.org/10.1371/journal.pgen.1004078	journal	January 2014
The Genome of the Generalist Plant Pathogen Fusarium avenaceum Is Enriched with Genes Involved in Redox, Signaling and Secondary Metabolism Lysøe, Erik; Harris, Linda J.; Walkowiak, Sean PLoS ONE, Vol. 9, Issue 11 https://doi.org/10.1371/journal.pone.0112703	journal	November 2014
The Arbuscular Mycorrhizal Symbiosis: Origin and Evolution of a Beneficial Plant Infection Corradi, Nicolas; Bonfante, Paola PLoS Pathogens, Vol. 8, Issue 4 https://doi.org/10.1371/journal.ppat.1002600	journal	April 2012
The Accessory Genome as a Cradle for Adaptive Evolution in Pathogens Croll, Daniel; McDonald, Bruce A. PLoS Pathogens, Vol. 8, Issue 4 https://doi.org/10.1371/journal.ppat.1002608	journal	April 2012
A Survey of the Gene Repertoire of Gigaspora rosea Unravels Conserved Features among Glomeromycota for Obligate Biotrophy Tang, Nianwu; San Clemente, Hélène; Roy, Sébastien Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.00233	journal	March 2016
The Comparison of Expressed Candidate Secreted Proteins from Two Arbuscular Mycorrhizal Fungi Unravels Common and Specific Molecular Tools to Invade Different Host Plants Kamel, Laurent; Tang, Nianwu; Malbreil, Mathilde Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.00124	journal	February 2017
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
Lipid transfer from plants to arbuscular mycorrhiza fungi Keymer, Andreas; Pimprikar, Priya; Wewer, Vera eLife, Vol. 6 https://doi.org/10.7554/eLife.29107	journal	July 2017

Cited By (29)

Genome Sequence and Antifungal Activity of Two Niche-Sharing Pseudomonas protegens Related Strains Isolated from Hydroponics Polano, Cesare; Martini, Marta; Savian, Francesco Microbial Ecology, Vol. 77, Issue 4 https://doi.org/10.1007/s00248-018-1238-5	journal	August 2018
Metabolome changes are induced in the arbuscular mycorrhizal fungus Gigaspora margarita by germination and by its bacterial endosymbiont Dearth, Stephen P.; Castro, Hector F.; Venice, Francesco Mycorrhiza, Vol. 28, Issue 5-6 https://doi.org/10.1007/s00572-018-0838-8	journal	June 2018
Building de novo reference genome assemblies of complex eukaryotic microorganisms from single nuclei Montoliu-Nerin, Merce; Sánchez-García, Marisol; Bergin, Claudia Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-58025-3	journal	January 2020
Evidence of non-tandemly repeated rDNAs and their intragenomic heterogeneity in Rhizophagus irregularis Maeda, Taro; Kobayashi, Yuuki; Kameoka, Hiromu Communications Biology, Vol. 1, Issue 1 https://doi.org/10.1038/s42003-018-0094-7	journal	July 2018
At the nexus of three kingdoms: the genome of the mycorrhizal fungus Gigaspora margarita provides insights into plant, endobacterial and fungal interactions Venice, Francesco; Ghignone, Stefano; Salvioli di Fossalunga, Alessandra Environmental Microbiology, Vol. 22, Issue 1 https://doi.org/10.1111/1462-2920.14827	journal	October 2019
Fungal evolution: major ecological adaptations and evolutionary transitions Naranjo‐Ortiz, Miguel A.; Gabaldón, Toni Biological Reviews https://doi.org/10.1111/brv.12510	journal	April 2019
Mycorrhizal types differ in ecophysiology and alter plant nutrition and soil processes Tedersoo, Leho; Bahram, Mohammad Biological Reviews, Vol. 94, Issue 5 https://doi.org/10.1111/brv.12538	journal	May 2019
Fungal functional ecology: bringing a trait‐based approach to plant‐associated fungi Zanne, Amy E.; Abarenkov, Kessy; Afkhami, Michelle E. Biological Reviews, Vol. 95, Issue 2 https://doi.org/10.1111/brv.12570	journal	November 2019
Does genotypic and species diversity of mycorrhizal plants and fungi affect ecosystem function? Hazard, Christina; Johnson, David New Phytologist, Vol. 220, Issue 4 https://doi.org/10.1111/nph.15010	journal	February 2018
Sex, plasticity, and biologically significant variation in one Glomeromycotina species Sanders, Ian R. New Phytologist, Vol. 220, Issue 4 https://doi.org/10.1111/nph.15049	journal	February 2018
Biodiversity of arbuscular mycorrhizal fungi and ecosystem function Powell, Jeff R.; Rillig, Matthias C. New Phytologist, Vol. 220, Issue 4 https://doi.org/10.1111/nph.15119	journal	March 2018
How do arbuscular mycorrhizal fungi handle phosphate? New insight into fine‐tuning of phosphate metabolism Ezawa, Tatsuhiro; Saito, Katsuharu New Phytologist, Vol. 220, Issue 4 https://doi.org/10.1111/nph.15187	journal	April 2018
Partner communication and role of nutrients in the arbuscular mycorrhizal symbiosis Lanfranco, Luisa; Fiorilli, Valentina; Gutjahr, Caroline New Phytologist, Vol. 220, Issue 4 https://doi.org/10.1111/nph.15230	journal	May 2018
Arbuscular mycorrhizal fungi: intraspecific diversity and pangenomes Mathieu, Stephanie; Cusant, Loïc; Roux, Christophe New Phytologist, Vol. 220, Issue 4 https://doi.org/10.1111/nph.15275	journal	June 2018
The future has roots in the past: the ideas and scientists that shaped mycorrhizal research Bonfante, Paola New Phytologist, Vol. 220, Issue 4 https://doi.org/10.1111/nph.15397	journal	August 2018
Genome and evolution of the arbuscular mycorrhizal fungus Diversispora epigaea (formerly Glomus versiforme ) and its bacterial endosymbionts Sun, Xuepeng; Chen, Wenbo; Ivanov, Sergey New Phytologist, Vol. 221, Issue 3 https://doi.org/10.1111/nph.15472	journal	October 2018
Arbuscular mycorrhizal fungi possess a CLAVATA3/embryo surrounding region‐related gene that positively regulates symbiosis Le Marquer, Morgane; Bécard, Guillaume; Frei dit Frey, Nicolas New Phytologist, Vol. 222, Issue 2 https://doi.org/10.1111/nph.15643	journal	January 2019
Comparative genomics of Rhizophagus irregularis , R. cerebriforme , R. diaphanus and Gigaspora rosea highlights specific genetic features in Glomeromycotina Morin, Emmanuelle; Miyauchi, Shingo; San Clemente, Hélène New Phytologist, Vol. 222, Issue 3 https://doi.org/10.1111/nph.15687	journal	February 2019
A lysin motif effector subverts chitin‐triggered immunity to facilitate arbuscular mycorrhizal symbiosis Zeng, Tian; Rodriguez‐Moreno, Luis; Mansurkhodzaev, Artem New Phytologist, Vol. 225, Issue 1 https://doi.org/10.1111/nph.16245	journal	November 2019
Identification of new signalling peptides through a genome-wide survey of 250 fungal secretomes Le Marquer, Morgane; San Clemente, Hélène; Roux, Christophe BMC Genomics, Vol. 20, Issue 1 https://doi.org/10.1186/s12864-018-5414-2	journal	January 2019
In silico analysis of fungal small RNA accumulation reveals putative plant mRNA targets in the symbiosis between an arbuscular mycorrhizal fungus and its host plant Silvestri, Alessandro; Fiorilli, Valentina; Miozzi, Laura BMC Genomics, Vol. 20, Issue 1 https://doi.org/10.1186/s12864-019-5561-0	journal	March 2019
To trade in the field: the molecular determinants of arbuscular mycorrhiza nutrient exchange Salvioli di Fossalunga, Alessandra; Novero, Mara Chemical and Biological Technologies in Agriculture, Vol. 6, Issue 1 https://doi.org/10.1186/s40538-019-0150-7	journal	June 2019
Arbuscular mycorrhizal fungi induce the expression of specific retrotransposons in roots of sunflower (Helianthus annuus L.) Vangelisti, Alberto; Mascagni, Flavia; Giordani, Tommaso PLOS ONE, Vol. 14, Issue 2 https://doi.org/10.1371/journal.pone.0212371	journal	February 2019
Investigating unexplained genetic variation and its expression in the arbuscular mycorrhizal fungus Rhizophagus irregularis: A comparison of whole genome and RAD sequencing data Masclaux, Frédéric G.; Wyss, Tania; Pagni, Marco PLOS ONE, Vol. 14, Issue 12 https://doi.org/10.1371/journal.pone.0226497	journal	December 2019
RiCRN1, a Crinkler Effector From the Arbuscular Mycorrhizal Fungus Rhizophagus irregularis, Functions in Arbuscule Development Voß, Stefanie; Betz, Ruben; Heidt, Sven Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.02068	journal	September 2018
Designing the Ideotype Mycorrhizal Symbionts for the Production of Healthy Food Avio, Luciano; Turrini, Alessandra; Giovannetti, Manuela Frontiers in Plant Science, Vol. 9 https://doi.org/10.3389/fpls.2018.01089	journal	August 2018
Beneficial Services of Arbuscular Mycorrhizal Fungi – From Ecology to Application Chen, Min; Arato, Miguel; Borghi, Lorenzo Frontiers in Plant Science, Vol. 9 https://doi.org/10.3389/fpls.2018.01270	journal	September 2018
Transcriptome Analysis of Wheat Roots Reveals a Differential Regulation of Stress Responses Related to Arbuscular Mycorrhizal Fungi and Soil Disturbance Campos, Catarina; Nobre, Tânia; Goss, Michael J. Biology, Vol. 8, Issue 4 https://doi.org/10.3390/biology8040093	journal	December 2019
Single nucleus sequencing reveals evidence of inter-nucleus recombination in arbuscular mycorrhizal fungi Chen, Eric CH; Mathieu, Stephanie; Hoffrichter, Anne eLife, Vol. 7 https://doi.org/10.7554/elife.39813	journal	December 2018

Similar Records

A dipeptide transporter from the arbuscular mycorrhizal fungus Rhizophagus irregularis is upregulated in the intraradical phase

Journal Article · Tue Sep 02 20:00:00 EDT 2014 · Frontiers in Plant Science · OSTI ID:1628261

Comparative genomics of Rhizophagus irregularis , R. cerebriforme , R. diaphanus and Gigaspora rosea highlights specific genetic features in Glomeromycotina

Journal Article · Sat Jan 12 19:00:00 EST 2019 · New Phytologist · OSTI ID:1619118

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Plant Sciences
Rhizophagus irregularis
arbuscular mycorrhizal fungi (AMF)
gene exchange
intraspecific variation
pan-genome
transposable elements

High intraspecific genome diversity in the model arbuscular mycorrhizal symbiont Rhizophagus irregularis

Citation Formats

References (73)

Cited By (29)

Similar Records

Related Subjects