A Survey of the gene repertoire of Gigaspora rosea unravels conserved features among glomeromycota for obligate biotrophy

Frontiers in Microbiology

Volumn 7, Issue MAR, 2016, Pages

  Tang, Nianwu ^a,b   San Clemente, Hélène ^b   Roy, Sébastien ^c   Bécard, Guillaume ^b   Zhao, Bin ^a   Roux, Christophe ^b  

^a HUAZHONG AGRICULTURAL UNIVERSITY   (China)

^b UNIVERSITÉ PAUL SABATIER   (France)

^c AGRONUTRITION Laboratoire de Biotechnologies   (France)

Author keywords

Arbuscular mycorrhizal fungi; Gene repertoire; Glomeromycota; MRNA sequencing; Obligate biotrophy; Phylogenomics

Indexed keywords

5' UNTRANSLATED REGION; ARBUSCULAR MYCORRHIZA; ARTICLE; BARREL MEDIC; BRACHYPODIUM; ENZYME DEGRADATION; FAS GENE; FUNGUS GROWTH; GENE; GENE EXPRESSION; GIGASPORA; GLOMEROMYCOTA; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; SIMPLE SEQUENCE REPEAT; SINGLE NUCLEOTIDE POLYMORPHISM;

EID: 84964329945     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2016.00233     Document Type: Article

References (140)

1. Akiyama, K., Matsuzaki, K., and Hayashi, H. (2005). Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435, 824-827. doi: 10.1038/nature03608
2. Amselem, J., Cuomo, C. A., van Kan, J. A. L., Viaud, M., Benito, E. P., Couloux, A., et al. (2011). Genomic analysis of the necrotrophic fungal pathogens Sclerotinia sclerotiorum and Botrytis cinerea. PLoS Genet. 7:e1002230. doi: 10.1371/journal.pgen.1002230
3. Arnaud, M. B., Cerqueira, G. C., Inglis, D. O., Skrzypek, M. S., Binkley, J., Chibucos, M. C., et al. (2012). The Aspergillus Genome Database (AspGD): recent developments in comprehensive multispecies curation, comparative genomics and community resources. Nucleic Acids Res. 40, D653-D659. doi: 10.1093/nar/gkr875
4. Aroca, R., Bago, A., Sutka, M., Paz, J. A., Cano, C., Amodeo, G., et al. (2009). Expression analysis of the first arbuscular mycorrhizal fungi aquaporin described reveals concerted gene expression between salt-stressed and nonstressed mycelium. Mol. Plant Microbe Interact. 22, 1169-1178. doi: 10.1094/MPMI-22-9-1169
5. Bécard, G., and Fortin, J. A. (1988). Early events of vesicular-arbuscular mycorrhiza formation on Ri T-DNA transformed roots. New Phytol. 108, 211-218. doi: 10.1111/j.1469-8137.1988.tb03698.x
6. Benedetto, A., Magurno, F., Bonfante, P., and Lanfranco, L. (2005). Expression profiles of a phosphate transporter gene (GmosPT) from the endomycorrhizal fungus Glomus mosseae. Mycorrhiza 15, 620-627. doi: 10.1007/s00572-005-0006-9
7. Besserer, A., Becard, G., Jauneau, A., Roux, C., and Sejalon-Delmas, N. (2008). GR24, a synthetic analog of strigolactones, stimulates the mitosis and growth of the arbuscular mycorrhizal fungus Gigaspora rosea by boosting its energy metabolism. Plant Physiol. 148, 402-413. doi: 10.1104/pp.108.121400
8. Besserer, A., Puech-Pagès, V., Kiefer, P., Gomez-Roldan, V., Jauneau, A., Roy, S., et al. (2006). Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria. PLoS Biol. 4:e226. doi: 10.1371/journal.pbio.0040226
9. Bever, J. D., Kang, H.-J., Kaonongbua, W., and Wang, M. (2008). "Genomic Organization and Mechanisms of Inheritance in Arbuscular Mycorrhizal Fungi: Contrasting the Evidence and Implications of Current Theories, "in Mycorrhiza: State of the Art, Genetics and Molecular Biology, Eco-Function, Biotechnology, Eco-Physiology, Structure and Systematics, ed. A. Varma (Berlin, Heidelberg: Springer Berlin Heidelberg), 135-148. doi: 10.1007/978-3-540-78826-3_7
10. Bidartondo, M. I., Read, D. J., Trappe, J. M., Merckx, V., Ligrone, R., and Duckett, J. G. (2011). The dawn of symbiosis between plants and fungi. Biol. Lett. 7, 574-577. doi: 10.1098/rsbl.2010.1203
11. Bonfante, P., and Genre, A. (2010). Mechanisms underlying beneficial plant-fungus interactions in mycorrhizal symbiosis. Nat. Commun. 1, 48. doi: 10.1038/ncomms1046
12. Boon, E., Halary, S., Bapteste, E., and Hijri, M. (2015). Studying genome heterogeneity within the arbuscular mycorrhizal fungal cytoplasm. Genome Biol. Evol. 7, 505-521. doi: 10.1093/gbe/evv002
13. Boon, E., Zimmerman, E., Lang, B. F., and Hijri, M. (2010). Intra-isolate genome variation in arbuscular mycorrhizal fungi persists in the transcriptome. J. Evol. Biol. 23, 1519-1527. doi: 10.1111/j.1420-9101.2010.02019.x
14. Braun, B. R., van Het Hoog, M., d'Enfert, C., Martchenko, M., Dungan, J., Kuo, A., et al. (2005). A human-curated annotation of the Candida albicans genome. PLoS Genet. 1:e1. doi: 10.1371/journal.pgen.0010001
15. Buee, M., Rossignol, M., Jauneau, A., Ranjeva, R., and Bécard, G. (2000). The pre-symbiotic growth of arbuscular mycorrhizal fungi is induced by a branching factor partially purified from plant root exudates. Mol. Plant Microbe Interact. 13, 693-698. doi: 10.1094/MPMI.2000.13.6.693
16. Castresana, J. (2000). Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol. Biol. Evol. 17, 540-552. doi: 10.1093/oxfordjournals.molbev.a026334
17. Cisse, O. H., Pagni, M., and Hauser, P. M. (2014). Comparative genomics suggests that the human pathogenic fungus Pneumocystis jirovecii acquired obligate biotrophy through gene loss. Genome Biol. Evol. 6, 1938-1948. doi: 10.1093/gbe/evu155
18. Clarke, P. R., and Zhang, C. (2001). Ran GTPase: a master regulator of nuclear structure and function during the eukaryotic cell division cycle? Trends Cell Biol. 11, 366-371. doi: 10.1016/S0962-8924(01)02071-2
19. Corradi, N., and Lildhar, L. (2012). Meiotic genes in the arbuscular mycorrhizal fungi. Commun. Integr. Biol. 5, 187-189. doi: 10.4161/cib.18850
20. Corradi, N., and Sanders, I. R. (2006). Evolution of the P-type II ATPase gene family in the fungi and presence of structural genomic changes among isolates of Glomus intraradices. BMC Evol. Biol. 6:21. doi: 10.1186/1471-2148-6-21
21. Costa De Oliveira, A., Da Maia, L. C., Palmieri, D. A., De Souza, V. Q., Kopp, M. M., and De Carvalho, F. I. F. (2008). SSR locator: tool for simple sequence repeat discovery integrated with primer design and PCR simulation. Int. J. Plant Genomics 2008, 412696-412705. doi: 10.1155/2008/412696
22. Croll, D., and Sanders, I. R. (2009). Recombination in Glomus intraradices, a supposed ancient asexual arbuscular mycorrhizal fungus. BMC Evol. Biol. 9:13. doi: 10.1186/1471-2148-9-13
23. Croll, D., Wille, L., Gamper, H. A., Mathimaran, N., Lammers, P. J., Corradi, N., et al. (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 Phytol. 178, 672-687. doi: 10.1111/j.1469-8137.2008.02381.x
24. Curtis, D. S., Phillips, A. R., Callister, S. J., Conlan, S., and McCue, L. A. (2013). SPOCS: software for predicting and visualizing orthology/paralogy relationships among genomes. Bioinformatics 29, 2641-2642. doi: 10.1093/bioinformatics/btt454
25. Dean, R. A., Talbot, N. J., Ebbole, D. J., Farman, M. L., Mitchell, T. K., Orbach, M. J., et al. (2005). The genome sequence of the rice blast fungus Magnaporthe grisea. Nature 434, 980-986. doi: 10.1038/nature03449
26. Desirò, A., Faccio, A., Kaech, A., Bidartondo, M. I., and Bonfante, P. (2015). Endogone, one of the oldest plant-associated fungi, host unique Mollicutes-related endobacteria. New Phytol. 205, 1464-1472. doi: 10.1111/nph.13136
27. Dickson, S., Smith, F. A., and Smith, S. E. (2007). Structural differences in arbuscular mycorrhizal symbioses: more than 100 years after Gallaud, where next? Mycorrhiza 17, 375-393. doi: 10.1007/s00572-007-0130-9
28. Dotzler, N., Krings, M., Taylor, T. N., and Agerer, R. (2006). Germination shields in Scutellospora (Glomeromycota: Diversisporales, Gigasporaceae) from the 400 million-year-old Rhynie chert. Mycol. Prog. 5, 178-184. doi: 10.1007/s11557-006-0511-z
29. Duplessis, S., Cuomo, C. A., Lin, Y.-C., Aerts, A., Tisserant, E., Veneault-Fourrey, C., et al. (2011). Obligate biotrophy features unraveled by the genomic analysis of rust fungi. Proc. Natl. Acad. Sci. U.S.A. 108, 9166-9171. doi: 10.1073/pnas.1019315108
30. Ellerbeck, M., Schübler, A., Brucker, D., Dafinger, C., Loos, F., and Brachmann, A. (2013). Characterization of three ammonium transporters of the glomeromycotan fungus Geosiphon pyriformis. Eukaryot. Cell 12, 1554-1562. doi: 10.1128/EC.00139-13
31. Emanuelsson, O., Brunak, S., von Heijne, G., and Nielsen, H. (2007). Locating proteins in the cell using TargetP, SignalP and related tools. Nat. Protoc. 2, 953-971. doi: 10.1038/nprot.2007.131
32. Fellbaum, C. R., Gachomo, E. W., Beesetty, Y., Choudhari, S., Strahan, G. D., Pfeffer, P. E., et al. (2012). Carbon availability triggers fungal nitrogen uptake and transport in arbuscular mycorrhizal symbiosis. Proc. Natl. Acad. Sci. U.S.A. 109, 2666-2671. doi: 10.1073/pnas.1118650109
33. Field, K. J., Rimington, W. R., Bidartondo, M. I., Allinson, K. E., Beerling, D. J., Cameron, D. D., et al. (2015). First evidence of mutualism between ancient plant lineages (Haplomitriopsida liverworts) and Mucoromycotina fungi and its response to simulated Palaeozoic changes in atmospheric CO 2. New Phytol. 205, 743-756. doi: 10.1111/nph.13024
34. Galagan, J. E., Calvo, S. E., Borkovich, K. A., Selker, E. U., Read, N. D., Jaffe, D., et al. (2003). The genome sequence of the filamentous fungus Neurospora crassa. Nature 422, 859-868. doi: 10.1038/nature01554
35. Galagan, J. E., Calvo, S. E., Cuomo, C., Ma, L.-J., Wortman, J. R., Batzoglou, S., et al. (2005). Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae. Nature 438, 1105-1115. doi: 10.1038/nature04341
36. Goffeau, A., Barrell, B. G., Bussey, H., Davis, R. W., Dujon, B., Feldmann, H., et al. (1996). Life with 6000 genes. Science 274, 563-567. doi: 10.1126/science.274.5287.546
37. Goyer, A. (2010). Thiamine in plants: aspects of its metabolism and functions. Phytochemistry 71, 1615-1624. doi: 10.1016/j.phytochem.2010.06.022
38. Guindon, S., Dufayard, J. F., Lefort, V., Anisimova, M., Hordijk, W., and Gascuel, O. (2010). New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59, 307-321. doi: 10.1093/sysbio/syq010
39. Gutjahr, C., and Parniske, M. (2013). Cell and developmental biology of arbuscular mycorrhiza symbiosis. Annu. Rev. Cell Dev. Biol. 29, 593-617. doi: 10.1146/annurev-cellbio-101512-122413
40. Guttman, D. S., McHardy, A. C., and Schulze-Lefert, P. (2014). Microbial genome-enabled insights into plant-microorganism interactions. Nat. Rev. Genet. 15, 797-813. doi: 10.1038/nrg3748
41. Halary, S., Malik, S. B., Lildhar, L., Slamovits, C. H., Hijri, M., and Corradi, N. (2011). Conserved meiotic machinery in Glomus spp., a putatively ancient asexual fungal lineage. Genome Biol. Evol. 3, 950-958. doi: 10.1093/gbe/evr089
42. Hane, J. K., Anderson, J. P., Williams, A. H., Sperschneider, J., and Singh, K. B. (2014). Genome sequencing and comparative genomics of the broad host-range pathogen Rhizoctonia solani AG8. PLoS Genet. 10:e1004281. doi: 10.1371/journal.pgen.1004281
43. Harrison, M. (2012). Cellular programs for arbuscular mycorrhizal symbiosis. Curr. Opin. Plant Biol. 15, 691-698. doi: 10.1016/j.pbi.2012.08.010
44. Harrison, M. J., and van Buuren, M. L. (1995). A phosphate transporter from the mycorrhizal fungus Glomus versiforme. Nature 378, 626-629. doi: 10.1038/378626a0
45. Helber, N., Wippel, K., Sauer, N., Schaarschmidt, S., Hause, B., and Requena, N. (2011). A versatile monosaccharide transporter that operates in the arbuscular mycorrhizal fungus glomus sp is crucial for the symbiotic relationship with plants. Plant Cell 23, 3812-3823. doi: 10.1105/tpc.111.089813
46. Hijri, M., and Sanders, I. R. (2005). Low gene copy number shows that arbuscular mycorrhizal fungi inherit genetically different nuclei. Nature 433, 160-163. doi: 10.1038/nature03069
47. Hosny, M., Gianinazzi-Pearson, V., and Dulieu, H. (1998). Nuclear DNA content of 11 fungal species in Glomales. Genome 41, 422-428. doi: 10.1139/gen-41-3-422
48. Humphreys, C. P., Franks, P. J., Rees, M., Bidartondo, M. I., Leake, J. R., and Beerling, D. J. (2010). Mutualistic mycorrhiza-like symbiosis in the most ancient group of land plants. Nat. Commun. 1, 103. doi: 10.1038/ncomms1105
49. Jakobsen, I., and Rosendahl, L. (1990). Carbon flow into soil and external hyphae from roots of mycorrhizal cucumber plants. New Phytol. 115, 77-83. doi: 10.1111/j.1469-8137.1990.tb00924.x
50. James, T. Y., Kauff, F., Schoch, C. L., Matheny, P. B., Hofstetter, V., Cox, C. J., et al. (2006). Reconstructing the early evolution of Fungi using a six-gene phylogeny. Nature 443, 818-822. doi: 10.1038/nature05110
51. Janbon, G., Ormerod, K. L., Paulet, D., Byrnes, E. J., Yadav, V., Chatterjee, G., et al. (2014). Analysis of the genome and transcriptome of Cryptococcus neoformans var. grubii reveals complex RNA expression and microevolution leading to virulence attenuation. PLoS Genet. 10:e1004261. doi: 10.1371/journal.pgen.1004261
52. Jones, T., Federspiel, N. A., Chibana, H., Dungan, J., Kalman, S., Magee, B. B., et al. (2004). The diploid genome sequence of Candida albicans. Proc. Natl. Acad. Sci. U.S.A. 101, 7329-7334. doi: 10.1073/pnas.0401648101
53. Kämper, J., Kahmann, R., Bölker, M., Ma, L.-J., Brefort, T., Saville, B. J., et al. (2006). Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 444, 97-101. doi: 10.1038/nature05248
54. Katoh, K., Misawa, K., Kuma, K., and Miyata, T. (2002). MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 30, 3059-3066. doi: 10.1093/nar/gkf436
55. Kelkar, Y. D., and Ochman, H. (2012). Causes and consequences of genome expansion in fungi. Genome Biol. Evol. 4, 13-23. doi: 10.1093/gbe/evr124
56. Kiers, E. T., Duhamel, M., Beesetty, Y., Mensah, J. A., Franken, O., Verbruggen, E., et al. (2011). Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333, 880-882. doi: 10.1126/science.1208473
57. Kloppholz, S., Kuhn, H., and Requena, N. (2011). A secreted fungal effector of Glomus intraradices promotes symbiotic biotrophy. Curr. Biol. 21, 1204-1209. doi: 10.1016/j.cub.2011.06.044
58. Kohler, A., Kuo, A., Nagy, L. G., Morin, E., Barry, K. W., Buscot, F., et al. (2015). Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists. Nat. Genet. 47, 410-415. doi: 10.1038/ng.3223
59. Kohlmeier, M. (2003). "Thiamin, "in Nutrient Metabolism, ed. M. Kohlmeier (London: Academic Press), 551-561. doi: 10.1016/B978-012417762-8.50080-6
60. Kovalchuk, A., Kohler, A., Martin, F., and Asiegbu, F. O. (2015). Diversity and evolution of ABC proteins in mycorrhiza-forming fungi. BMC Evol. Biol. 15:1. doi: 10.1186/s12862-015-0526-7
61. Krüger, M., Krüger, C., Walker, C., Stockinger, H., and Schübler, A. (2012). Phylogenetic reference data for systematics and phylotaxonomy of arbuscular mycorrhizal fungi from phylum to species level. New Phytol. 193, 970-984. doi: 10.1111/j.1469-8137.2011.03962.x
62. Kuhn, G., Hijri, M., and Sanders, I. R. (2001). Evidence for the evolution of multiple genomes in arbuscular mycorrhizal fungi. Nature 414, 745-748. doi: 10.1038/414745a
63. Lanfranco, L., Novero, M., and Bonfante, P. (2005). The mycorrhizal fungus Gigaspora margarita possesses a CuZn superoxide dismutase that is up-regulated during symbiosis with legume hosts. Plant Physiol. 137, 1319-1330. doi: 10.1104/pp.104.050435
64. Lanfranco, L., and Young, J. P. W. (2012). Genetic and genomic glimpses of the elusive arbuscular mycorrhizal fungi. Curr. Opin. Plant Biol. 15, 454-461. doi: 10.1016/j.pbi.2012.04.003
65. Lee, J., and Young, J. P. W. (2009). The mitochondrial genome sequence of the arbuscular mycorrhizal fungus Glomus intraradices isolate 494 and implications for the phylogenetic placement of Glomus. New Phytol. 183, 200-211. doi: 10.1111/j.1469-8137.2009.02834.x
66. Li, T., Hu, Y.-J., Hao, Z.-P., Li, H., Wang, Y.-S., and Chen, B.-D. (2013). First cloning and characterization of two functional aquaporin genes from an arbuscular mycorrhizal fungus Glomus intraradices. New Phytol. 197, 617-630. doi: 10.1111/nph.12011
67. Li, W., and Godzik, A. (2006). Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22, 1658-1659. doi: 10.1093/bioinformatics/btl158
68. Lin, K., Limpens, E., Zhang, Z., Ivanov, S., Saunders, D. G. O., Mu, D., et al. (2014). Single nucleus genome sequencing reveals high similarity among nuclei of an endomycorrhizal fungus. PLoS Genet. 10:e1004078. doi: 10.1371/journal.pgen.1004078
69. Liu, Y., Leigh, J. W., Brinkmann, H., Cushion, M. T., Rodriguez-Ezpeleta, N., Philippe, H., et al. (2009). Phylogenomic analyses support the monophyly of taphrinomycotina, including Schizosaccharomyces fission yeasts. Mol. Biol. Evol. 26, 27-34. doi: 10.1093/molbev/msn221
70. Liu, Y. J., Hodson, M. C., and Hall, B. D. (2006). Loss of the flagellum happened only once in the fungal lineage: phylogenetic structure of kingdom Fungi inferred from RNA polymerase II subunit genes. BMC Evol. Biol. 6:74. doi: 10.1186/1471-2148-6-74
71. Longato, S., and Bonfante, P. (1997). Molecular identification of mycorrhizal fungi by direct amplification of microsatellite regions. Mycol. Res. 101, 425-432. doi: 10.1017/S0953756296002766
72. López-Pedrosa, A., González-Guerrero, M., Valderas, A., Azcón-Aguilar, C., and Ferrol, N. (2006). GintAMT1 encodes a functional high-affinity ammonium transporter that is expressed in the extraradical mycelium of Glomus intraradices. Fungal Genet. Biol. 43, 102-110. doi: 10.1016/j.fgb.2005.10.005
73. Ma, L. J., Ibrahim, A. S., Skory, C., Grabherr, M. G., Burger, G., Butler, M., et al. (2009). Genomic analysis of the basal lineage fungus Rhizopus oryzae reveals a whole-genome duplication. PLoS Genet. 5:e1000549. doi: 10.1371/journal.pgen.1000549
74. Maherali, H., and Klironomos, J. N. (2007). Influence of phylogeny on fungal community assembly and ecosystem functioning. Science 316, 1746-1748. doi: 10.1126/science.1143082
75. Maldonado-Mendoza, I. E., Dewbre, G. R., and Harrison, M. J. (2001). A phosphate transporter gene from the extra-radical mycelium of an arbuscular mycorrhizal fungus Glomus intraradices is regulated in response to phosphate in the environment. Mol. Plant Microbe Interact. 14, 1140-1148. doi: 10.1094/MPMI.2001.14.10.1140
76. Malinovsky, F. G., Fangel, J. U., and Willats, W. G. T. (2014). The role of the cell wall in plant immunity. Front. Plant Sci. 5:178. doi: 10.3389/fpls.2014.00178
77. Martin, F., Aerts, A., Ahrén, D., Brun, A., Danchin, E. G. J., Duchaussoy, F., et al. (2008). The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature 452, 88-92. doi: 10.1038/nature06556
78. Martin, F., Kohler, A., Murat, C., Balestrini, R., Coutinho, P. M., Jaillon, O., et al. (2010). Périgord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis. Nature 464, 1033-1038. doi: 10.1038/nature08867
79. Mathimaran, N., Falquet, L., Ineichen, K., Picard, C., Redecker, D., Boller, T., et al. (2008). Microsatellites for disentangling underground networks: strain-specific identification of Glomus intraradices, an arbuscular mycorrhizal fungus. Fungal Genet. Biol. 45, 812-817. doi: 10.1016/j.fgb.2008.02.009
80. Meinken, J., Asch, D. K., Neizer-ashun, K. A., Chang, G. H., Cooper, C. R. Jr., and Min, X. J. (2014). FunSecKB2: a fungal protein subcellular location knowledgebase. Comput. Mol. Biol. 4, 1-17. doi: 10.5376/cmb.2014.04.0007
81. Milne, I., Lindner, D., Bayer, M., Husmeier, D., Mcguire, G., Marshall, D. F., et al. (2009). TOPALi v2: a rich graphical interface for evolutionary analyses of multiple alignments on HPC clusters and multi-core desktops. Bioinformatics 25, 126-127. doi: 10.1093/bioinformatics/btn575
82. Min, X. J., Butler, G., Storms, R., and Tsang, A. (2005). OrfPredictor: predicting protein-coding regions in EST-derived sequences. Nucleic Acids Res. 33, 677-680. doi: 10.1093/nar/gki394
83. Moriya, Y., Itoh, M., Okuda, S., Yoshizawa, A. C., and Kanehisa, M. (2007). KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res. 35, 182-185. doi: 10.1093/nar/gkm321
84. Nadimi, M., Beaudet, D., Forget, L., Hijri, M., and Franz Lang, B. (2012). Group i intron-mediated trans-splicing in mitochondria of gigaspora rosea and a robust phylogenetic affiliation of arbuscular mycorrhizal fungi with mortierellales. Mol. Biol. Evol. 29, 2199-2210. doi: 10.1093/molbev/mss088
85. Nordberg, H., Cantor, M., Dusheyko, S., Hua, S., Poliakov, A., Shabalov, I., et al. (2014). The genome portal of the department of energy joint genome institute: 2014 updates. Nucleic Acids Res. 42, D26-D31. doi: 10.1093/nar/gkt1069
86. Öpik, M., Vanatoa, A., Vanatoa, E., Moora, M., Davison, J., Kalwij, J. M., et al. (2010). The online database MaarjAM reveals global and ecosystemic distribution patterns in arbuscular mycorrhizal fungi (Glomeromycota). New Phytol. 188, 223-241. doi: 10.1111/j.1469-8137.2010.03334.x
87. Pao, S. S., Paulsen, I. T., and Saier, M. H. (1998). Major facilitator superfamily. Microbiol. Mol. Biol. Rev. 62, 1-34
88. Park, J., Park, J., Jang, S., Kim, S., Kong, S., Choi, J., et al. (2008). FTFD: an informatics pipeline supporting phylogenomic analysis of fungal transcription factors. Bioinformatics 24, 1024-1025. doi: 10.1093/bioinformatics/btn058
89. Parniske, M. (2008). Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat. Rev. Microbiol. 6, 763-775. doi: 10.1038/nrmicro1987
90. Parra, G., Bradnam, K., Ning, Z., Keane, T., and Korf, I. (2009). Assessing the gene space in draft genomes. Nucleic Acids Res. 37, 289-297. doi: 10.1093/nar/gkn916
91. Parrent, J. L., James, T. Y., Vasaitis, R., and Taylor, A. F. (2009). Friend or foe? Evolutionary history of glycoside hydrolase family 32 genes encoding for sucrolytic activity in fungi and its implications for plant-fungal symbioses. BMC Evol. Biol. 9:148. doi: 10.1186/1471-2148-9-148
92. Pawlowska, T. E. (2005). Genetic processes in arbuscular mycorrhizal fungi. FEMS Microbiol. Lett. 251, 185-192. doi: 10.1016/j.femsle.2005.08.007
93. Pawlowska, T. E., and Taylor, J. W. (2004). Organization of genetic variation in individuals of arbuscular mycorrhizal fungi. Nature 427, 733-737. doi: 10.1038/nature02290
94. Pérez-Tienda, J., Testillano, P. S., Balestrini, R., Fiorilli, V., Azcón-Aguilar, C., and Ferrol, N. (2011). GintAMT2, a new member of the ammonium transporter family in the arbuscular mycorrhizal fungus Glomus intraradices. Fungal Genet. Biol. 48, 1044-1055. doi: 10.1016/j.fgb.2011.08.003
95. Pfeffer, P. E., Douds, D. D., Bécard, G., and Shachar-Hill, Y. (1999). Carbon uptake and the metabolism and transport of lipids in an arbuscular mycorrhiza. Plant Physiol. 120, 587-598. doi: 10.1104/pp.120.2.587
96. Quevillon, E., Silventoinen, V., Pillai, S., Harte, N., Mulder, N., Apweiler, R., et al. (2005). InterProScan: protein domains identifier. Nucleic Acids Res. 33, 116-120. doi: 10.1093/nar/gki442
97. Rasmussen, A., Heugebaert, T., Matthys, C., Van Deun, R., Boyer, F. D., Goormachtig, S., et al. (2013). A fluorescent alternative to the synthetic strigolactone GR24. Mol. Plant 6, 100-112. doi: 10.1093/mp/sss110
98. Rees, D. C., Johnson, E., and Lewinson, O. (2009). ABC transporters: the power to change. Nat. Rev. Mol. Cell Biol. 10, 218-227. doi: 10.1038/nrm2646.ABC
99. Remy, W., Taylor, T. N., Hass, H., and Kerp, H. (1994). Four hundred-million-year-old vesicular arbuscular mycorrhizae. Proc. Natl. Acad. Sci. U.S.A. 91, 11841-11843. doi: 10.1073/pnas.91.25.11841
100. Riley, R., Charron, P., Idnurm, A., Farinelli, L., Dalpé, Y., Martin, F., et al. (2014). Extreme diversification of the mating type-high-mobility group (MATA-HMG) gene family in a plant-associated arbuscular mycorrhizal fungus. New Phytol. 201, 254-268. doi: 10.1111/nph.12462
101. Riley, R., and Corradi, N. (2013). Searching for clues of sexual reproduction in the genomes of arbuscular mycorrhizal fungi. Fungal Ecol. 6, 44-49. doi: 10.1016/j.funeco.2012.01.010
102. Rimington, W. R., Pressel, S., Duckett, J. G., and Bidartondo, M. I. (2015). Fungal associations of basal vascular plants: reopening a closed book? New Phytol. 205, 1394-1398. doi: 10.1111/nph.13221
103. Ronquist, F., and Huelsenbeck, J. P. (2003). MrBayes 3: bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572-1574. doi: 10.1093/bioinformatics/btg180
104. Salvioli, A., Ghignone, S., Novero, M., Navazio, L., Venice, F., Bagnaresi, P., et al. (2016). Symbiosis with an endobacterium increases the fitness of a mycorrhizal fungus, raising its bioenergetic potential. ISME J. 10, 130-144. doi: 10.1038/ismej.2015.91
105. Sanders, I. R. (2003). Preference, specicity and cheating in the arbuscular mycorrhizal symbiosis. Trends Plant Sci. 8, 143-145. doi: 10.1016/S1360-1385(03)00012-8
106. Sanders, I. R., and Croll, D. (2010). Arbuscular mycorrhiza: the challenge to understand the genetics of the fungal partner. Annu. Rev. Genet. 44, 271-292. doi: 10.1146/annurev-genet-102108-134239
107. Sawers, R. J. H., Gutjahr, C., and Paszkowski, U. (2008). Cereal mycorrhiza: an ancient symbiosis in modern agriculture. Trends Plant Sci. 13, 93-97. doi: 10.1016/j.tplants.2007.11.006
108. Schaarschmidt, S., González, M.-C., Roitsch, T., Strack, D., Sonnewald, U., and Hause, B. (2007a). Regulation of arbuscular mycorrhization by carbon. The symbiotic interaction cannot be improved by increased carbon availability accomplished by root-specifically enhanced invertase activity. Plant Physiol. 143, 1827-1840. doi: 10.1104/pp.106.096446
109. Schaarschmidt, S., Kopka, J., Ludwig-Müller, J., and Hause, B. (2007b). Regulation of arbuscular mycorrhization by apoplastic invertases: enhanced invertase activity in the leaf apoplast affects the symbiotic interaction. Plant J. 51, 390-405. doi: 10.1111/j.1365-313X.2007.03150.x
110. Schaarschmidt, S., Roitsch, T., and Hause, B. (2006). Arbuscular mycorrhiza induces gene expression of the apoplastic invertase LIN6 in tomato (Lycopersicon esculentum) roots. J. Exp. Bot. 57, 4015-4023. doi: 10.1093/jxb/erl172
111. Schübler, A., Schwarzott, D., and Walker, C. (2001). A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol. Res. 105, 1413-1421. doi: 10.1017/S0953756201005196
112. Schüssler, A., Martin, H., Cohen, D., Fitz, M., and Wipf, D. (2006). Characterization of a carbohydrate transporter from symbiotic glomeromycotan fungi. Nature 444, 933-936. doi: 10.1038/nature05364
113. Seedzielewska, K. A., Fuchs, J., Temsch, E. M., Baronian, K., Watzke, R., and Kunze, G. (2011). Estimation of the Glomus intraradices nuclear DNA content. New Phytol. 192, 794-797. doi: 10.1111/j.1469-8137.2011.03937.x
114. Shelest, E. (2008). Transcription factors in fungi. FEMS Microbiol. Lett. 286, 145-151. doi: 10.1111/j.1574-6968.2008.01293.x
115. Simão, F. A., Waterhouse, R. M., Ioannidis, P., and Kriventseva, E. V. (2015). BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31, 3210-3212. doi: 10.1093/bioinformatics/btv351
116. Smith, S. E., and Read, D. J. (1997). Mycorrhizal Symbiosis, 2nd Edn. London: Academic Press
117. Smith, S. E., and Read, D. J. (2008). Mycorrhizal Symbiosis, 3rd Edn. London: Academic Press
118. Spanu, P. D., Abbott, J. C., Amselem, J., Burgis, T. A., Soanes, D. M., Stüber, K., et al. (2010). Genome expansion and gene loss in powdery mildew fungi reveal tradeoffs in extreme parasitism. Science 330, 1543-1546. doi: 10.1126/science.1194573
119. Staats, M., and van Kan, J. A. L. (2012). Genome update of Botrytis cinerea strains B05.10 and T4. Eukaryot. Cell 11, 1413-1414. doi: 10.1128/EC.00164-12
120. Stajich, J. E., Wilke, S. K., Ahren, D., Au, C. H., Birren, B. W., Borodovsky, M., et al. (2010). Insights into evolution of multicellular fungi from the assembled chromosomes of the mushroom Coprinopsis cinerea (Coprinus cinereus). Proc. Natl. Acad. Sci. U.S.A. 107, 11889-11894. doi: 10.1073/pnas.1003391107
121. Strack, D., and Fester, T. (2006). Isoprenoid metabolism and plastid reorganization in arbuscular mycorrhizal roots. New Phytol. 172, 22-34. doi: 10.1111/j.1469-8137.2006.01837.x
122. Stukenbrock, E. H., and Rosendahl, S. (2005). Clonal diversity and population genetic structure of arbuscular mycorrhizal fungi (Glomus spp.) studied by multilocus genotyping of single spores. Mol. Ecol. 14, 743-752. doi: 10.1111/j.1365-294X.2005.02453.x
123. Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S. (2013). MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30, 2725-2729. doi: 10.1093/molbev/mst197
124. Tauzin, A. S., and Giardina, T. (2014). Sucrose and invertases, a part of the plant defense response to the biotic stresses. Front. Plant Sci. 5:293. doi: 10.3389/fpls.2014.00293
125. Tian, C., Kasiborski, B., Koul, R., Lammers, P. J., Bucking, H., and 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 Physiol. 153, 1175-1187. doi: 10.1104/pp.110.156430
126. Tisserant, E., Kohler, A., Dozolme-Seddas, P., Balestrini, R., Benabdellah, K., Colard, A., et al. (2012). The transcriptome of the arbuscular mycorrhizal fungus Glomus intraradices (DAOM 197198) reveals functional tradeoffs in an obligate symbiont. New Phytol. 193, 755-769. doi: 10.1111/j.1469-8137.2011.03948.x
127. Tisserant, E., Malbreil, M., Kuo, A., Kohler, A., Symeonidi, A., Balestrini, R., et al. (2013). Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis. Proc. Natl. Acad. Sci. U.S.A. 110, 20117-20122. doi: 10.1073/pnas.1313452110
128. Todd, R. B., Zhou, M., Ohm, R. A., Leeggangers, H. A. C. F., Visser, L., and de Vries, R. P. (2014). Prevalence of transcription factors in ascomycete and basidiomycete fungi. BMC Genomics 15:214. doi: 10.1186/1471-2164-15-214
129. Tollot, M., Wong Sak Hoi, J., Van Tuinen, D., Arnould, C., Chatagnier, O., Dumas, B., et al. (2009). An STE12 gene identified in the mycorrhizal fungus Glomus intraradices restores infectivity of a hemibiotrophic plant pathogen. New Phytol. 181, 693-707. doi: 10.1111/j.1469-8137.2008.02696.x
130. Trépanier, M., Bécard, G., Moutoglis, P., Willemot, C., Gagné, S., Avis, T. J., et al. (2005). Dependence of arbuscular-mycorrhizal fungi on their plant host for palmitic acid synthesis. Appl. Environ. Microbiol. 71, 5341-5347. doi: 10.1128/AEM.71.9.5341
131. Turrà, D., El Ghalid, M., Rossi, F., and Di Pietro, A. (2015). Fungal pathogen uses sex pheromone receptor for chemotropic sensing of host plant signals. Nature 527, 521-524. doi: 10.1038/nature15516
132. Wang, E., Schornack, S., Marsh, J. F., Gobbato, E., Schwessinger, B., Eastmond, P., et al. (2012). A common signaling process that promotes mycorrhizal and oomycete colonization of plants. Curr. Biol. 22, 2242-2246. doi: 10.1016/j.cub.2012.09.043
133. Wang, X., Zhang, X., Liu, L., Xiang, M., Wang, W., Sun, X., et al. (2015). Genomic and transcriptomic analysis of the endophytic fungus Pestalotiopsis fici reveals its lifestyle and high potential for synthesis of natural products. BMC Genomics 16:28. doi: 10.1186/s12864-014-1190-9
134. Wewer, V., Brands, M., and Dörmann, P. (2014). Fatty acid synthesis and lipid metabolism in the obligate biotrophic fungus Rhizophagus irregularis during mycorrhization of Lotus japonicus. Plant J. 79, 398-412. doi: 10.1111/tpj.12566
135. Winnenburg, R., Baldwin, T. K., Urban, M., Rawlings, C., Köhler, J., and Hammond-Kosack, K. E. (2006). PHI-base: a new database for pathogen host interactions. Nucleic Acids Res. 34, D459-D464. doi: 10.1093/nar/gkj047
136. Wood, V., Gwilliam, R., Rajandream, M.-A., Lyne, M., Lyne, R., Stewart, A., et al. (2002). The genome sequence of Schizosaccharomyces pombe. Nature 415, 871-880. doi: 10.1038/nature724
137. Wood, V., Harris, M. A., McDowall, M. D., Rutherford, K., Vaughan, B. W., Staines, D. M., et al. (2012). PomBase: a comprehensive online resource for fission yeast. Nucleic Acids Res. 40, D695-D699. doi: 10.1093/nar/gkr853
138. Wu, S., Zhu, Z., Fu, L., Niu, B., and Li, W. (2011). WebMGA: a customizable web server for fast metagenomic sequence analysis. BMC Genomics 12:444. doi: 10.1186/1471-2164-12-444
139. Yin, Y., Mao, X., Yang, J., Chen, X., Mao, F., and Xu, Y. (2012). dbCAN: a web resource for automated carbohydrate-active enzyme annotation. Nucleic Acids Res. 40, W445-W451. doi: 10.1093/nar/gks479
140. Zuccaro, A., Lahrmann, U., Güldener, U., Langen, G., Pfiffi, S., Biedenkopf, D., et al. (2011). Endophytic life strategies decoded by genome and transcriptome analyses of the mutualistic root symbiont Piriformospora indica. PLoS Pathog. 7:e1002290. doi: 10.1371/journal.ppat.1002290