title: The transcriptome of the arbuscular mycorrhizal fungus Glomus intraradices (DAOM 197198) reveals functional tradeoffs in an obligate symbiont.
abstract: • The arbuscular mycorrhizal symbiosis is arguably the most ecologically important eukaryotic symbiosis, yet it is poorly understood at the molecular level. To provide novel insights into the molecular basis of symbiosis-associated traits, we report the first genome-wide analysis of the transcriptome from Glomus intraradices DAOM 197198. • We generated a set of 25,906 nonredundant virtual transcripts (NRVTs) transcribed in germinated spores, extraradical mycelium and symbiotic roots using Sanger and 454 sequencing. NRVTs were used to construct an oligoarray for investigating gene expression. • We identified transcripts coding for the meiotic recombination machinery, as well as meiosis-specific proteins, suggesting that the lack of a known sexual cycle in G. intraradices is not a result of major deletions of genes essential for sexual reproduction and meiosis. Induced expression of genes encoding membrane transporters and small secreted proteins in intraradical mycelium, together with the lack of expression of hydrolytic enzymes acting on plant cell wall polysaccharides, are all features of G. intraradices that are shared with ectomycorrhizal symbionts and obligate biotrophic pathogens. • Our results illuminate the genetic basis of symbiosis-related traits of the most ancient lineage of plant biotrophs, advancing future research on these agriculturally and ecologically important symbionts.
authors.affiliation: Institut National de la Recherche Agronomique (INRA), UMR 1136 INRA/University Henri Poincaré, Interactions Arbres/Micro-organismes, Centre de Nancy, 54280 Champenoux, France.
authors.forename: E
authors.initials: E
authors.lastname: Tisserant
authors.affiliation: Institut National de la Recherche Agronomique (INRA), UMR 1136 INRA/University Henri Poincaré, Interactions Arbres/Micro-organismes, Centre de Nancy, 54280 Champenoux, France.
authors.forename: A
authors.initials: A
authors.lastname: Kohler
authors.affiliation: UMR 1088 INRA/5184 CNRS/Burgundy University Plante-Microbe-Environnement, INRA-CMSE, BP 86510, 21065 Dijon, France.
authors.forename: P
authors.initials: P
authors.lastname: Dozolme-Seddas
authors.affiliation: Istituto per la Protezione delle Piante del CNR, sez. di Torino and Dipartimento di Biologia Vegetale, Universita` degli Studi di Torino, Viale Mattioli, 25, 10125 Torino, Italy.
authors.forename: R
authors.initials: R
authors.lastname: Balestrini
authors.affiliation: Departamento de Microbiología del Suelo y Sistemas Simbióticos, Estación Experimental del Zaidín, CSIC, C. Profesor Albareda, 1, 18008 Granada, Spain.
authors.forename: K
authors.initials: K
authors.lastname: Benabdellah
authors.affiliation: Department of Ecology and Evolution, University of Lausanne, Biophore Building, 1015 Lausanne, Switzerland.|ETH Zürich, Plant Pathology, Universitätsstrasse 3, CH-8092 Zürich, Switzerland.
authors.forename: A
authors.initials: A
authors.lastname: Colard
authors.affiliation: Department of Ecology and Evolution, University of Lausanne, Biophore Building, 1015 Lausanne, Switzerland.|ETH Zürich, Plant Pathology, Universitätsstrasse 3, CH-8092 Zürich, Switzerland.
authors.forename: D
authors.initials: D
authors.lastname: Croll
authors.affiliation: CEA, IG, Genoscope, 2 rue Gaston Crémieux CP5702, F-91057 Evry, France.
authors.forename: C
authors.initials: C
authors.lastname: Da Silva
authors.affiliation: Boyce Thompson Institute for Plant Research, Tower Road, Ithaca, NY 14853-1801, USA.
authors.forename: S K
authors.initials: SK
authors.lastname: Gomez
authors.affiliation: Department of Chemistry and Biochemistry, New Mexico State University, Department 3MLS, PO Box 3001, Las Cruces, NM 88003-8001, USA.
authors.forename: R
authors.initials: R
authors.lastname: Koul
authors.affiliation: Departamento de Microbiología del Suelo y Sistemas Simbióticos, Estación Experimental del Zaidín, CSIC, C. Profesor Albareda, 1, 18008 Granada, Spain.
authors.forename: N
authors.initials: N
authors.lastname: Ferrol
authors.affiliation: Istituto per la Protezione delle Piante del CNR, sez. di Torino and Dipartimento di Biologia Vegetale, Universita` degli Studi di Torino, Viale Mattioli, 25, 10125 Torino, Italy.
authors.forename: V
authors.initials: V
authors.lastname: Fiorilli
authors.affiliation: Université de Toulouse & CNRS, UPS, UMR 5546, Laboratoire de Recherche en Sciences Végétales, BP 42617, F-31326, Castanet-Tolosan, France.
authors.forename: D
authors.initials: D
authors.lastname: Formey
authors.affiliation: Leibniz-Institute of Vegetable and Ornamental Crops, Department of Plant Nutrition, Theodor-Echtermeyer-Weg 1, D-14979 Grossbeeren, Germany.
authors.forename: Ph
authors.initials: P
authors.lastname: Franken
authors.affiliation: Karlsruhe Institute of Technology, Botanical Institute, Plant-Microbial Interaction, Hertzstrasse 16, D-76187 Karlsruhe, Germany.
authors.forename: N
authors.initials: N
authors.lastname: Helber
authors.affiliation: Institut de la Recherche en Biologie Végétale, Département de sciences biologiques, Université de Montréal, 4101 Rue Sherbrooke est, Montréal, Que., Canada H1X 2B2.
authors.forename: M
authors.initials: M
authors.lastname: Hijri
authors.affiliation: Istituto per la Protezione delle Piante del CNR, sez. di Torino and Dipartimento di Biologia Vegetale, Universita` degli Studi di Torino, Viale Mattioli, 25, 10125 Torino, Italy.
authors.forename: L
authors.initials: L
authors.lastname: Lanfranco
authors.affiliation: Joint Genome Institute, 2800 Mitchell Drive, Walnut Creek, CA 94598, USA.
authors.forename: E
authors.initials: E
authors.lastname: Lindquist
authors.affiliation: UMR 1088 INRA/5184 CNRS/Burgundy University Plante-Microbe-Environnement, INRA-CMSE, BP 86510, 21065 Dijon, France.
authors.forename: Y
authors.initials: Y
authors.lastname: Liu
authors.affiliation: Université de Toulouse & CNRS, UPS, UMR 5546, Laboratoire de Recherche en Sciences Végétales, BP 42617, F-31326, Castanet-Tolosan, France.
authors.forename: M
authors.initials: M
authors.lastname: Malbreil
authors.affiliation: Institut National de la Recherche Agronomique (INRA), UMR 1136 INRA/University Henri Poincaré, Interactions Arbres/Micro-organismes, Centre de Nancy, 54280 Champenoux, France.
authors.forename: E
authors.initials: E
authors.lastname: Morin
authors.affiliation: CEA, IG, Genoscope, 2 rue Gaston Crémieux CP5702, F-91057 Evry, France.
authors.forename: J
authors.initials: J
authors.lastname: Poulain
authors.affiliation: Joint Genome Institute, 2800 Mitchell Drive, Walnut Creek, CA 94598, USA.
authors.forename: H
authors.initials: H
authors.lastname: Shapiro
authors.affiliation: UMR 1088 INRA/5184 CNRS/Burgundy University Plante-Microbe-Environnement, INRA-CMSE, BP 86510, 21065 Dijon, France.
authors.forename: D
authors.initials: D
authors.lastname: van Tuinen
authors.affiliation: Leibniz-Institute of Vegetable and Ornamental Crops, Department of Plant Nutrition, Theodor-Echtermeyer-Weg 1, D-14979 Grossbeeren, Germany.
authors.forename: A
authors.initials: A
authors.lastname: Waschke
authors.affiliation: Departamento de Microbiología del Suelo y Sistemas Simbióticos, Estación Experimental del Zaidín, CSIC, C. Profesor Albareda, 1, 18008 Granada, Spain.
authors.forename: C
authors.initials: C
authors.lastname: Azcón-Aguilar
authors.affiliation: Université de Toulouse & CNRS, UPS, UMR 5546, Laboratoire de Recherche en Sciences Végétales, BP 42617, F-31326, Castanet-Tolosan, France.
authors.forename: G
authors.initials: G
authors.lastname: Bécard
authors.affiliation: Istituto per la Protezione delle Piante del CNR, sez. di Torino and Dipartimento di Biologia Vegetale, Universita` degli Studi di Torino, Viale Mattioli, 25, 10125 Torino, Italy.
authors.forename: P
authors.initials: P
authors.lastname: Bonfante
authors.affiliation: Boyce Thompson Institute for Plant Research, Tower Road, Ithaca, NY 14853-1801, USA.
authors.forename: M J
authors.initials: MJ
authors.lastname: Harrison
authors.affiliation: Institut für Pflanzengenetik, Naturwissenschaftliche Fakultät, Leibniz Universität Hannover, D-30419 Hannover, Germany.
authors.forename: H
authors.initials: H
authors.lastname: Küster
authors.affiliation: Department of Chemistry and Biochemistry, New Mexico State University, Department 3MLS, PO Box 3001, Las Cruces, NM 88003-8001, USA.
authors.forename: P
authors.initials: P
authors.lastname: Lammers
authors.affiliation: Department de Biologie Moléculaire Végétale, Université de Lausanne, Biophore, 4419, CH-1015 Lausanne, Switzerland.
authors.forename: U
authors.initials: U
authors.lastname: Paszkowski
authors.affiliation: Karlsruhe Institute of Technology, Botanical Institute, Plant-Microbial Interaction, Hertzstrasse 16, D-76187 Karlsruhe, Germany.
authors.forename: N
authors.initials: N
authors.lastname: Requena
authors.affiliation: BIOSS Centre for Biological Signalling Studies, Freiburg Initiative for Systems Biology and Faculty of Biology, University of Freiburg, Hauptstr. 1, D-79104 Freiburg, Germany.
authors.forename: S A
authors.initials: SA
authors.lastname: Rensing
authors.affiliation: Université de Toulouse & CNRS, UPS, UMR 5546, Laboratoire de Recherche en Sciences Végétales, BP 42617, F-31326, Castanet-Tolosan, France.
authors.forename: C
authors.initials: C
authors.lastname: Roux
authors.affiliation: Department of Ecology and Evolution, University of Lausanne, Biophore Building, 1015 Lausanne, Switzerland.
authors.forename: I R
authors.initials: IR
authors.lastname: Sanders
authors.affiliation: Department of Plant Biology, Michigan State University, East Lansing, MI 48824-1312, USA.
authors.forename: Y
authors.initials: Y
authors.lastname: Shachar-Hill
authors.affiliation: Oak Ridge National Laboratory, BioSciences, PO Box 2008, Oak Ridge, TN 37831, USA.
authors.forename: G
authors.initials: G
authors.lastname: Tuskan
authors.affiliation: Department of Biology, University of York, York YO10 5DD, UK.
authors.forename: J P W
authors.initials: JPW
authors.lastname: Young
authors.affiliation: UMR 1088 INRA/5184 CNRS/Burgundy University Plante-Microbe-Environnement, INRA-CMSE, BP 86510, 21065 Dijon, France.
authors.forename: V
authors.initials: V
authors.lastname: Gianinazzi-Pearson
authors.affiliation: Institut National de la Recherche Agronomique (INRA), UMR 1136 INRA/University Henri Poincaré, Interactions Arbres/Micro-organismes, Centre de Nancy, 54280 Champenoux, France.
authors.forename: F
authors.initials: F
authors.lastname: Martin
mesh_terms: D001483:Base Sequence; D015169:Colony Count, Microbial; D005656:Fungal Proteins / Q000737:chemistry / Q000235:genetics / Q000378:metabolism; D015966:Gene Expression Regulation, Fungal; D015723:Gene Library; D005800:Genes, Fungal / Q000235:genetics; D055137:Glomeromycota / Q000235:genetics* / Q000254:growth & development; D008540:Meiosis / Q000235:genetics; D025282:Mycelium / Q000235:genetics; D038821:Mycorrhizae / Q000235:genetics* / Q000254:growth & development; D010944:Plants / Q000382:microbiology; D020641:Polymorphism, Single Nucleotide / Q000235:genetics; D017434:Protein Structure, Tertiary; D012333:RNA, Messenger / Q000235:genetics / Q000378:metabolism; D013559:Symbiosis / Q000235:genetics*; D059467:Transcriptome / Q000235:genetics*; D015854:Up-Regulation / Q000235:genetics
chemical_list: D005656:Fungal Proteins; D012333:RNA, Messenger
references.citation: Akiyama K, Matsuzaki KI, Hayashi H. 2005. Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435: 824-827.
references.citation: Allen JW, Shachar-Hill Y. 2009. Sulfur transfer through an arbuscular mycorrhiza. Plant Physiology 149: 549-560.
references.citation: Angelard C, Colard A, Niculita-Hirzel H, Croll D, Sanders IR. 2010. Segregation in a mycorrhizal fungus alters rice growth and symbiosis-specific gene transcription. Current Biology 20: 1216-1221.
references.citation: Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT et al. 2000. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nature Genetics 25: 25-29.
references.citation: Audic S, Claverie JM. 1997. The significance of digital gene expression profiles. Genome Research 7: 986-995.
references.citation: Bago B, Pfeffer PE, Abubaker J, Jun J, Allen JW, Brouillette J, Douds DD, Lammers PJ, Shachar-Hill Y. 2003. Carbon export from arbuscular mycorrhizal roots involves the translocation of carbohydrate as well as lipid. Plant Physiology 131: 1496-1507.
references.citation: Bago B, Pfeffer PE, Shachar-Hill Y. 2000. Carbon metabolism and transport in arbuscular mycorrhizas. Plant Physiology 124: 949-957.
references.citation: Balestrini R, Gómez-Ariza J, Lanfranco L, Bonfante P. 2007. Laser microdissection reveals that transcripts for five plant and one fungal phosphate transporter genes are contemporaneously present in arbusculated cells. Molecular Plant-Microbe Interactions 20: 1055-1062.
references.citation: Balestrini R, Lanfranco L. 2006. Fungal and plant gene expression in arbuscular mycorrhizal symbiosis. Mycorrhiza 16: 509-524.
references.citation: Baxter L, Tripathy S, Ishaque N, Boot N, Cabral A, Kemen E, Thines M, Ah-Fong A, Anderson R, Badejoko W et al. 2010. Signatures of adaptation to obligate biotrophy in the Hyaloperonospora arabidopsidis genome. Science 330: 1549-1551.
references.citation: Bécard G, Fortin JA. 1988. Early events of vesicular arbuscular mycorrhiza formation on Ri T-DNA transformed roots. New Phytologist 108: 211-218.
references.citation: Bécard G, Kosuta S, Tamasloukht M, Séjalon-Delmas N, Roux C. 2004. Partner communication in the arbuscular mycorrhizal interaction. Canadian Journal of Botany 8: 1186-1197.
references.citation: Bendtsen JD, Nielsen H, von Heijne G, Brunak S. 2004. Improved prediction of signal peptides: SignalP 3.0. Journal of Molecular Biology 340: 783-795.
references.citation: Benedetto A, Magurno F, Bonfante P, Lanfranco L. 2005. Expression profiles of a phosphate transporter gene (GmosPT) from the endomycorrhizal fungus Glomus mosseae. Mycorrhiza 15: 620-627.
references.citation: Bonfante P, Genre A. 2010. Mechanisms underlying beneficial plant-fungus interactions in mycorrhizal symbiosis. Nature Communications 1: 48.
references.citation: Cantarel BL, Continho PM, Rancurel C, Bernard T, Lombard V, Henrissat B. 2009. The Carbohydrate-Active enzymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Research 37: D233-D238.
references.citation: Chabot S, Bécard G, Piché Y. 1992. The life cycle of Glomus intraradices in root organ culture. Mycologia 84: 315-321.
references.citation: Chevreux B, Pfisterer T, Drescher B, Driesel AJ, Müller WEG, Wetter T, Suhai S. 2004. Using the miraEST assembler for reliable and automated mRNA transcript assembly and SNP detection in sequenced ESTs. Genome Research 14: 1147-1159.
references.citation: Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M. 2005. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21: 3674-3676.
references.citation: Croll D, Giovannetti M, Koch AM, Sbrana C, Ehinger M, Lammers PJ, Sanders IR. 2009. Nonself vegetative fusion and genetic exchange in the arbuscular mycorrhizal fungus Glomus intraradices. New Phytologist 181: 924-937.
references.citation: Croll D, Sanders IR. 2009. Recombination in Glomus intraradices, a supposed ancient asexual arbuscular mycorrhizal fungus. BMC Evolutionary Biology 9: 13.
references.citation: Croll D, Wille L, Gamper HA, Mathimaran N, Lammers PJ, Corradi N, Sanders IR. 2008. Genetic diversity and host plant preferences revealed by simple sequence repeat and mitochondrial markers in a population of the arbuscular mycorrhizal fungus Glomus intraradices. New Phytologist 178: 672-687.
references.citation: De Wit PJGM, Mehrabi R, Van Den Burg HA, Stergiopoulos I. 2009. Fungal effector proteins: past, present and future. Molecular Plant Pathology 10: 735-747.
references.citation: Dodds PN, Rathjen JP. 2010. Plant immunity: towards an integrated view of plant-pathogen interactions. Nature Reviews Genetics 8: 539-548.
references.citation: Duplessis S, Cuomo CA, Lin YC, Aerts A, Tisserant E, Veneault-Fourrey C, Joly DL, Hacquard S, Amselem J, Cantarel BL et al. 2011. Obligate biotrophy features unraveled by the genomic analysis of the rust fungi, Melampsora larici-populina and Puccinia graminis f. sp. tritici. Proceedings of the National Academy of Sciences, USA 108: 9166-9171.
references.citation: Emanuelsson O, Nielsen H, Brunak S, von Heijne G. 2000. Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. Journal of Molecular Biology 300: 1005-1016.
references.citation: Ercolin F, Reinhardt D. 2011. Successful joint ventures of plants: arbuscular mycorrhiza and beyond. Trends in Plant Science 16: 356-362.
references.citation: Fitter AH, Helgason T, Hodge A. 2011. Nutritional exchanges in the arbuscular mycorrhizal symbiosis: implications for sustainable agriculture. Fungal Biology Reviews 25: 68-72.
references.citation: Genre A, Chabaud M, Timmers T, Bonfante P, Barker DG. 2005. Arbuscular mycorrhizal fungi elicit a novel intracellular apparatus in Medicago truncatula root epidermal cells before infection. Plant Cell 17: 3489-3499.
references.citation: Giovannetti M, Fortuna P, Citernesi AS, Morini S, Nuti MP. 2001. The occurrence of anastomosis formation and nuclear exchange in intact arbuscular mycorrhizal networks. New Phytologist 151: 717-724.
references.citation: Gomez SK, Javot H, Deewatthanawong P, Torres-Jerez I, Tang Y, Blancaflor EB, Udvardi MK, Harrison MJ. 2009. Medicago truncatula and Glomus intraradices gene expression in cortical cells harboring arbuscules in the arbuscular mycorrhizal symbiosis. BMC Plant Biology 22: 10.
references.citation: Gómez-Ariza J, Balestrini R, Novero M, Bonfante P. 2009. Cell-specific gene expression of phosphate transporters in mycorrhizal tomato roots. Biology and Fertility of Soils 45: 845-853.
references.citation: Govindarajulu M, Pfeffer PE, Jin HR, Abubaker J, Douds DD, Allen JW, Bucking H, Lammers PJ, Shachar-Hill Y. 2005. Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 435: 819-823.
references.citation: Grunwald U, Guo W, Fischer K, Isayenkov S, Ludwig-Müller J, Hause B, Yan X, Küster H, Franken P. 2009. Overlapping expression patterns and differential transcript levels of phosphate transporter genes in arbuscular mycorrhizal, Pi-fertilised and phytohormone-treated Medicago truncatula roots. Planta 229: 1023-1034.
references.citation: Guether M, Balestrini R, Hannah MA, Udvardi MK, Bonfante P. 2009a. Genome-wide reprogramming of regulatory networks, transport, cell wall and membrane biogenesis during arbuscular mycorrhizal symbiosis in Lotus japonicus. New Phytologist 182: 200-212.
references.citation: Guether M, Neuhäuser B, Balestrini R, Dynowski M, Ludewig U, Bonfante P. 2009b. A mycorrhizal-specific ammonium transporter from Lotus japonicus acquires nitrogen released by arbuscular mycorrhizal fungi. Plant Physiology 150: 73-83.
references.citation: Güimil S, Chang H-S, Zhu T, Sesma A, Osbourn A, Roux C, Ioannidis V, Oakeley EJ, Docquier M, Descombes P et al. 2005. Comparative transcriptomics of rice reveals an ancient pattern of response to microbial colonization. Proceedings of the National Academy of Sciences, USA 102: 8066-8070.
references.citation: Halary S, Malik SB, Lildhar L, Slamovits CH, Hijri M, Corradi N. 2011. Conserved meiotic machinery in Glomus spp., a putatively ancient asexual fungal lineage. Genome Biology and Evolution 3: 950-958.
references.citation: van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR. 1998. Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396: 69-72.
references.citation: Hijikata N, Murase M, Tani C, Ohtomo R, Osaki M, Ezawa T. 2010. Polyphosphate has a central role in the rapid and massive accumulation of phosphorus in extraradical mycelium of an arbuscular mycorrhizal fungus. New Phytologist 186: 285-289.
references.citation: Hothorn M, Neumann H, Lenherr ED, Wehner M, Rybin V, Hassa PO, Uttenweiler A, Reinhardt M, Schmidt A, Seiler J et al. 2009. Catalytic core of a membrane-associated eukaryotic polyphosphate polymerase. Science 324: 513-516.
references.citation: Idnurm A, Walton FJ, Floyd A, Heitman J. 2008. Identification of the sex genes in an early diverged fungus. Nature 451: 193-197.
references.citation: Jany JL, Pawlowska TE. 2010. Multinucleate spores contribute to evolutionary longevity of asexual Glomeromycota. The American Naturalist 175: 424-435.
references.citation: Javot H, Pumplin N, Harrison MJ. 2007. Phosphate in the arbuscular mycorrhizal symbiosis: transport properties and regulatory roles. Plant, Cell & Environment 30: 310-322.
references.citation: Kamoun S. 2007. Groovy times: filamentous pathogen effectors revealed. Current Opinion in Plant Biology 10: 358-365.
references.citation: Kanehisa M, Goto S. 2000. KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Research 28: 27-30.
references.citation: Kemen E, Gardiner A, Schultz-Larsen T, Kemen AC, Balmuth AL, Robert-Seilaniantz A, Bailey K, Holub E, Studholme DJ, Maclean D et al. 2011. Gene gain and loss during evolution of obligate parasitism in the white rust pathogen of Arabidopsis thaliana. PLoS Biology 9: e1001094.
references.citation: Kiers ET, Duhamel M, Beesetty Y, Mensah JA, Franken O, Verbruggen E, Fellbaum CR, Kowalchuk GA, Hart MM, Bago A et al. 2011. Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333: 880-882.
references.citation: Kloppholz S, Kuhn H, Requena N. 2011. A secreted fungal effector of Glomus intraradices promotes symbiotic biothrophy. Current Biology 21: 1204-1209.
references.citation: Krogh A, Larsson B, von Heijne G, Sonnhammer EL. 2001. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. Journal of Molecular Biology 305: 567-580.
references.citation: Kuhn H, Küster H, Requena N. 2010. Membrane steroid-binding protein 1 induced by a diffusible fungal signal is critical for mycorrhization in Medicago truncatula. New Phytologist 185: 716-733.
references.citation: Kuznetsova E, Seddas-Dozolme PMA, Arnould C, Tollot M, van Tuinen D, Borisov A, Gianinazzi S, Gianinazzi-Pearson V. 2010. Symbiosis-related pea genes modulate fungal and plant gene expression during the arbuscule stage of mycorrhiza with Glomus intraradices. Mycorrhiza 20: 427-443.
references.citation: Letunic I, Yamada T, Kanehisa M, Bork P. 2008. iPath: interactive exploration of biochemical pathways and networks. Trends in Biochemical Sciences 33: 101-103.
references.citation: Maere S, Heymans K, Kuiper M. 2005. BiNGO: a Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics 21: 3448-3449.
references.citation: Maillet F, Poinsot V, André O, Puech-Pagès V, Haouy A, Gueunier M, Cromer L, Giraudet D, Formey D, Niebel A et al. 2011. Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469: 58-63.
references.citation: Malik SB, Pightling AW, Stefaniak LM, Schurko AM, Logsdon JM. 2008. An expanded inventory of conserved meiotic genes provides evidence for sex in Trichomonas vaginalis. PLoS ONE 3: e2879.
references.citation: Martin F, Aerts A, Ahren D, Brun A, Danchin EGJ, Duchaussoy F, Gibon J, Kohler A, Lindquist E, Pereda V et al. 2008b. The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature 452: 88-92.
references.citation: Martin F, Gianinazzi-Pearson V, Hijri M, Lammers P, Requena N, Sanders IR, Shachar-Hill Y, Shapiro H, Tuskan GA, Young JPW. 2008a. The long hard road to a completed Glomus intraradices genome. New Phytologist 180: 747-750.
references.citation: Martin F, Kohler A, Murat C, Balestrini R, Coutinho PM, Jaillon O, Montanini B, Morin E, Noel B, Percudani R et al. 2010. Périgord Black Truffle genome uncovers evolutionary origins and mechanisms of symbiosis. Nature 464: 1033-1038.
references.citation: Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M. 2007. KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Research 35: W182-W185.
references.citation: Nagendran S, Hallen-Adams HE, Paper JM, Aslam N, Walton JD. 2009. Reduced genomic potential for secreted plant cell-wall-degrading enzymes in the ectomycorrhizal fungus Amanita bisporigera, based on the secretome of Trichoderma reesei. Fungal Genetics and Biology 46: 427-435.
references.citation: Parra G, Bradnam K, Ning Z, Keane T, Korf I. 2009. Assessing the gene space in draft genomes. Nucleic Acids Research 37: 289-297.
references.citation: Pérez-Tienda J, Testillano PS, Balestrini R, Fiorilli V, Azcón-Aguilar C, Ferrol N. 2011. GintAMT2, a new member of the ammonium transporter family in the arbuscular mycorrhizal fungus Glomus intraradices. Fungal Genetics and Biology 48: 1044-1055.
references.citation: Plett JM, Kemppainen M, Kale SD, Kohler A, Legué V, Brun A, Tyler B, Pardo A, Martin F. 2011. A secreted effector protein of Laccaria bicolor is required for symbiosis development. Current Biology 21: 1197-1203.
references.citation: Plett JM, Martin F. 2011. Blurred boundaries: lifestyle lessons from ectomycorrhizal fungal genomes. Trends in Genetics 27: 14-22.
references.citation: Rosendahl S. 2008. Communities, populations and individuals of arbuscular mycorrhizal fungi. New Phytologist 178: 253-266.
references.citation: Saeed AI, Bhagabati NK, Braisted JC, Liang W, Sharov V, Howe EA, Li J, Thiagarajan M, White JA, Quackenbush J. 2006. TM4 microarray software suite. Methods in Enzymology 411: 134-193.
references.citation: Sanders IR, Croll D. 2010. Arbuscular mycorrhiza: the challenge to understand the genetics of the fungal partner. Annual Review of Genetics 44: 271-292.
references.citation: Schaarschmidt S, Roitsch T, Hause B. 2006. Arbuscular mycorrhiza induces gene expression of the apoplastic invertase LIN6 in tomato (Lycopersicon esculentum) roots. Journal of Experimental Botany 57: 4015-4023.
references.citation: Schüssler A, Schwarzott D, Walker C. 2001. A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycological Research 105: 1413-1421.
references.citation: Schwanhäusser B, Busse D, Li N, Dittmar G, Schuchhardt J, Wolf J, Chen W, Selbach M. 2011. Global quantification of mammalian gene expression control. Nature 473: 337-342.
references.citation: Seddas PM, Arias C, Arnould C, van Tuinen D, Godfroy O, Benhassou H, Gouzy J, Morandi D, Dessaint F, Gianinazzi-Pearson V. 2009. Symbiosis-related plant genes modulate molecular responses in an arbuscular mycorrhizal fungus during early root interactions. Molecular Plant-Microbe Interactions 22: 341-351.
references.citation: Smith SE, Read DJ. 2008. Mycorrhizal symbiosis. London, UK: Academic press.
references.citation: Smith SE, Smith FA. 2011. Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annual Review of Plant Biology 62: 227-250.
references.citation: Spanu PD, Abbott JC, Amselem J, Burgis TA, Soanes DM, Stüber K, van Themaat EVL, Brown JKM, Butcher SA, Gurr SJ et al. 2010. Genome expansion and gene loss in powdery mildew fungi reveal tradeoffs in extreme parasitism. Science 330: 1543-1546.
references.citation: Stockinger H, Walker C, Schüßler A. 2009. ‘Glomus intraradices DAOM197198’, a model fungus in arbuscular mycorrhiza research, is not Glomus intraradices. New Phytologist 183: 1176-1187.
references.citation: Tani C, Ohtomo R, Osaki M, Kuga Y, Ezawa T. 2009. ATP-dependent but proton gradient-independent polyphosphate-synthesizing activity in extraradical hyphae of an arbuscular mycorrhizal fungus. Applied and Environmental Microbiology 75: 7044-7050.
references.citation: Tatusov RL, Fedorova ND, Jackson JD, Jacobs AR, Kiryutin B, Koonin EV, Krylov DM, Mazumder R, Mekhedov SL, Nikolskaya AN et al. 2003. The COG database: an updated version includes eukaryotes. BMC Bioinformatics 4: 41.
references.citation: Tian C, Kasiborski B, Koul R, Lammers PJ, Bucking H, Shachar-Hill Y. 2010. Regulation of the nitrogen transfer pathway in the arbuscular mycorrhizal symbiosis: gene characterization and the coordination of expression with nitrogen flux. Plant Physiology 153: 1175-1187.
references.citation: Viereck N, Hansen PE, Jakobsen I. 2004. Phosphate pool dynamics in the arbuscular mycorrhizal fungus Glomus intraradices studied by in vivo31P NMR spectroscopy. New Phytologist 162: 783-794.