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      Comparative genomics reveals high biological diversity and specific adaptations in the industrially and medically important fungal genus Aspergillus

      research-article
        1 , 2 , , 3 , 1 , 2 , 4 , 5 , 6 , 60 , 7 , 8 , 9 , 61 , 3 , 1 , 2 , 10 , 11 , 1 , 2 , 10 , 6 , 12 , 13 , 14 , 15 , 16 , 16 , 3 , 3 , 6 , 6 , 17 , 5 , 18 , 8 , 8 , 10 , 19 , 20 , 62 , 21 , 22 , 23 , 63 , 22 , 24 , 25 , 26 , 21 , 27 , 28 , 29 , 64 , 8 , 30 , 7 , 3 , 10 , 31 , 32 , 3 , 9 , 3 , 65 , 33 , 66 , 3 , 3 , 34 , 35 , 26 , 36 , 37 , 67 , 38 , 13 , 68 , 18 , 39 , 8 , 34 , 3 , 35 , 1 , 18 , 9 , 69 , 27 , 40 , 34 , 33 , 70 , 9 , 27 , 9 , 41 , 42 , 33 , 6 , 1 , 42 , 6 , 3 , 21 , 43 , 1 , 44 , 41 , 9 , 71 , 45 , 46 , 47 , 20 , 6 , 3 , 34 , 48 , 49 , 29 , 1 , 9 , 72 , 6 , 50 , 1 , 51 , 1 , 2 , 50 , 21 , 52 , 1 , 2 , 74 , 53 , 10 , 42 , 50 , 54 , 1 , 55 , 18 , 56 , 57 , 58 , 1 , 9 , 59 , 73 , 21 , 3
      Genome Biology
      BioMed Central
      Aspergillus, Genome sequencing, Comparative genomics, Fungal biology

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          Abstract

          Background

          The fungal genus Aspergillus is of critical importance to humankind. Species include those with industrial applications, important pathogens of humans, animals and crops, a source of potent carcinogenic contaminants of food, and an important genetic model. The genome sequences of eight aspergilli have already been explored to investigate aspects of fungal biology, raising questions about evolution and specialization within this genus.

          Results

          We have generated genome sequences for ten novel, highly diverse Aspergillus species and compared these in detail to sister and more distant genera. Comparative studies of key aspects of fungal biology, including primary and secondary metabolism, stress response, biomass degradation, and signal transduction, revealed both conservation and diversity among the species. Observed genomic differences were validated with experimental studies. This revealed several highlights, such as the potential for sex in asexual species, organic acid production genes being a key feature of black aspergilli, alternative approaches for degrading plant biomass, and indications for the genetic basis of stress response. A genome-wide phylogenetic analysis demonstrated in detail the relationship of the newly genome sequenced species with other aspergilli.

          Conclusions

          Many aspects of biological differences between fungal species cannot be explained by current knowledge obtained from genome sequences. The comparative genomics and experimental study, presented here, allows for the first time a genus-wide view of the biological diversity of the aspergilli and in many, but not all, cases linked genome differences to phenotype. Insights gained could be exploited for biotechnological and medical applications of fungi.

          Electronic supplementary material

          The online version of this article (doi:10.1186/s13059-017-1151-0) contains supplementary material, which is available to authorized users.

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          Most cited references235

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          tRNAscan-SE: A Program for Improved Detection of Transfer RNA Genes in Genomic Sequence

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            Gene prediction in novel fungal genomes using an ab initio algorithm with unsupervised training.

            We describe a new ab initio algorithm, GeneMark-ES version 2, that identifies protein-coding genes in fungal genomes. The algorithm does not require a predetermined training set to estimate parameters of the underlying hidden Markov model (HMM). Instead, the anonymous genomic sequence in question is used as an input for iterative unsupervised training. The algorithm extends our previously developed method tested on genomes of Arabidopsis thaliana, Caenorhabditis elegans, and Drosophila melanogaster. To better reflect features of fungal gene organization, we enhanced the intron submodel to accommodate sequences with and without branch point sites. This design enables the algorithm to work equally well for species with the kinds of variations in splicing mechanisms seen in the fungal phyla Ascomycota, Basidiomycota, and Zygomycota. Upon self-training, the intron submodel switches on in several steps to reach its full complexity. We demonstrate that the algorithm accuracy, both at the exon and the whole gene level, is favorably compared to the accuracy of gene finders that employ supervised training. Application of the new method to known fungal genomes indicates substantial improvement over existing annotations. By eliminating the effort necessary to build comprehensive training sets, the new algorithm can streamline and accelerate the process of annotation in a large number of fungal genome sequencing projects.
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              Ab initio gene finding in Drosophila genomic DNA.

              Ab initio gene identification in the genomic sequence of Drosophila melanogaster was obtained using (human gene predictor) and Fgenesh programs that have organism-specific parameters for human, Drosophila, plants, yeast, and nematode. We did not use information about cDNA/EST in most predictions to model a real situation for finding new genes because information about complete cDNA is often absent or based on very small partial fragments. We investigated the accuracy of gene prediction on different levels and designed several schemes to predict an unambiguous set of genes (annotation CGG1), a set of reliable exons (annotation CGG2), and the most complete set of exons (annotation CGG3). For 49 genes, protein products of which have clear homologs in protein databases, predictions were recomputed by Fgenesh+ program. The first annotation serves as the optimal computational description of new sequence to be presented in a database. Reliable exons from the second annotation serve as good candidates for selecting the PCR primers for experimental work for gene structure verification. Our results shows that we can identify approximately 90% of coding nucleotides with 20% false positives. At the exon level we accurately predicted 65% of exons and 89% including overlapping exons with 49% false positives. Optimizing accuracy of prediction, we designed a gene identification scheme using Fgenesh, which provided sensitivity (Sn) = 98% and specificity (Sp) = 86% at the base level, Sn = 81% (97% including overlapping exons) and Sp = 58% at the exon level and Sn = 72% and Sp = 39% at the gene level (estimating sensitivity on std1 set and specificity on std3 set). In general, these results showed that computational gene prediction can be a reliable tool for annotating new genomic sequences, giving accurate information on 90% of coding sequences with 14% false positives. However, exact gene prediction (especially at the gene level) needs additional improvement using gene prediction algorithms. The program was also tested for predicting genes of human Chromosome 22 (the last variant of Fgenesh can analyze the whole chromosome sequence). This analysis has demonstrated that the 88% of manually annotated exons in Chromosome 22 were among the ab initio predicted exons. The suite of gene identification programs is available through the WWW server of Computational Genomics Group at http://genomic.sanger.ac.uk/gf. html.
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                Author and article information

                Contributors
                r.devries@cbs.knaw.nl
                rwriley@lbl.gov
                a.wiebenga@cbs.knaw.nl
                gao@unam.mx
                samillis@biol.uoa.gr
                cris.uchima@gmail.com
                gregor.anderluh@ki.si
                assadollahi.m@gmail.com
                marion.askin@csiro.au
                kwbarry@lbl.gov
                evy.battaglia@cbs.knaw.nl
                ozgur.bayram@nuim.ie
                t.benocci@cbs.knaw.nl
                sbraus@gwdg.de
                camila.caldana@bioetanol.org.br
                davidc@us.es
                gustavo@broadinstitute.org
                chenfs@mail.hzau.edu.cn
                chenwanping@mail.hzau.edu.cn
                Cindy.choi@roche.com
                aclum@lbl.gov
                renatoacsantos@gmail.com
                adamasio@unicamp.br
                diallina@biol.uoa.gr
                emri.tamas@science.unideb.hu
                kicsizsoka@yahoo.com
                drir.michelflipphi@gmail.com
                susi.freyberg@gmail.com
                antonia.gallo@ispa.cnr.it
                Christos.Gournas@ulb.ac.be
                stxrhh@exmail.nottingham.ac.uk
                matthieu.hainaut@afmb.univ-mrs.fr
                mlharispe@gmail.com
                bernard.henrissat@afmb.univ-mrs.fr
                kristiina.s.hilden@helsinki.fi
                stxrjh@exmail.nottingham.ac.uk
                abeer.hossain@ddna-biotech.com
                me01519@cc.uoi.gr
                karaffa.levente@science.unideb.hu
                karanyi.zsolt@med.unideb.hu
                nada.krasevec@ki.si
                akuo@lbl.gov
                harald.kusch@med.uni-goettingen.de
                klabutti@lbl.gov
                Elagendijk@koppert.nl
                piterlabs@gmail.com
                anthony.levasseur@univ-amu.fr
                EALindquist@lbl.gov
                alipzen@lbl.gov
                antonio.logrieco@ispa.cnr.it
                andrew@iata.csic.es
                miia.r.makela@helsinki.fi
                imalavazi@ufscar.br
                petter.melin@icloud.com
                vera.meyer@tu-berlin.de
                natmiel@yahoo.com
                mm@internal.med.unideb.hu
                molnar.akos@science.unideb.hu
                giuseppina.mule@ispa.cnr.it
                Chewyee.Ngan@jax.org
                morejas@iata.csic.es
                orosz.zsoka@gmail.com
                jpaul_oued@yahoo.fr
                Karin.overkamp@ddna-biotech.com
                phsoo97@gmail.com
                giancarlo.perrone@ispa.cnr.it
                francois.piumi@jouy.inra.fr
                peter.punt@ddna-biotech.com
                A.F.J.Ram@biology.leidenuniv.nl
                anaramon@fcien.edu.uy
                Stefan.Rauscher@gmx.de
                eric.record@univ-amu.fr
                diego.riano@bioetanol.org.br
                v.robert@cbs.knaw.nl
                julian.roehrig@novartis.com
                roberto.ruller@bioetanol.org.br
                aasalamov@lbl.gov
                sbxns1@nottingham.ac.uk
                r.samson@cbs.knaw.nl
                karaffa@agr.unideb.hu
                msanguinetti@fcien.edu.uy
                tabea.schuetze@tu-berlin.de
                Kristina.Sepcic@bf.uni-lj.si
                ekaterina.shelest@leibniz-hki.de
                gsherloc@stanford.edu
                vicky@bio.demokritos.gr
                fabio.squina@bioetanol.org.br
                antonella.susca@ispa.cnr.it
                rbtodd@ksu.edu
                adrian.tsang@concordia.ca
                su@st-andrews.ac.uk
                n.vdwiele@bio-aware.com
                Diana.vanRossen@baseclear.nl
                juliana.velasco@bioetanol.org.br
                tcve@bio.dtu.dk
                j.visser@cbs.knaw.nl
                jyu1@wisc.edu
                miaomiaozhou88@hotmail.com
                mr@bio.dtu.dk
                david.archer@nottingham.ac.uk
                scott.baker@pnnl.gov
                i.benoit@cbs.knaw.nl
                axel.brakhage@leibniz-hki.de
                gbraus@gwdg.de
                reinhard.fischer@kit.edu
                jcf@bio.dtu.dk
                ggoldman@usp.br
                j.houbraken@cbs.knaw.nl
                boakley@ku.edu
                pocsi.istvan@science.unideb.hu
                c.scazzocchio@imperial.ac.uk
                bernhard.seiboth@tuwien.ac.at
                pavankuyk@yahoo.com.au
                jwortman@serestherapeutics.com
                paul.dyer@nottingham.ac.uk
                ivgrigoriev@lbl.gov
                Journal
                Genome Biol
                Genome Biol
                Genome Biology
                BioMed Central (London )
                1474-7596
                1474-760X
                14 February 2017
                14 February 2017
                2017
                : 18
                : 28
                Affiliations
                [1 ]Westerdijk Fungal Biodiversity Institute, Uppsalalaan 8, 3584 CT Utrecht, The Netherlands
                [2 ]ISNI 0000000120346234, GRID grid.5477.1, Fungal Molecular Physiology, , Utrecht University, ; Uppsalalaan 8, 3584 CT Utrecht, The Netherlands
                [3 ]ISNI 0000 0004 0449 479X, GRID grid.451309.a, , US Department of Energy Joint Genome Institute, ; 2800 Mitchell Drive, Walnut Creek, CA 94598 USA
                [4 ]ISNI 0000 0001 2159 0001, GRID grid.9486.3, Department of Food Science and Biotechnology, Faculty of Chemistry, , National University of Mexico, ; Ciudad Universitaria, D.F. C.P. 04510 Mexico
                [5 ]ISNI 0000 0001 2155 0800, GRID grid.5216.0, Department of Biology, , National and Kapodistrian University of Athens, ; Panepistimioupolis, 15781 Athens, Greece
                [6 ]ISNI 0000 0004 0445 0877, GRID grid.452567.7, Laboratório Nacional de Ciência e Tecnologia do Bioetanol (CTBE), , Centro Nacional de Pesquisa em Energia e Materiais (CNPEM), ; Caixa Postal 6192 CEP 13083-970, Campinas, São Paulo Brasil
                [7 ]ISNI 0000 0001 0661 0844, GRID grid.454324.0, Laboratory for Molecular Biology and Nanobiotechnology, , National Institute of Chemistry, ; Hajdrihova 19, 1000 Ljubljana, Slovenia
                [8 ]ISNI 0000 0001 1088 8582, GRID grid.7122.6, Department of Biochemical Engineering, Faculty of Science and Technology, , University of Debrecen, ; 4032 Debrecen, Hungary
                [9 ]ISNI 0000 0001 2312 1970, GRID grid.5132.5, , Institute of Biology Leiden, Molecular Microbiology and Biotechnology, Leiden University, ; Sylviusweg 72, 2333 BE Leiden, The Netherlands
                [10 ]ISNI 0000 0001 2364 4210, GRID grid.7450.6, Department of Molecular Microbiology and Genetics, , Institute for Microbiology and Genetics, Georg August University Göttingen, ; Grisebachstr. 8, 37077 Göttingen, Germany
                [11 ]ISNI 0000 0000 9331 9029, GRID grid.95004.38, Department of Biology, , Maynooth University, ; Maynooth, Co. Kildare Ireland
                [12 ]Max Planck Partner Group, Brazilian Bioethanol Science and Technology Laboratory, CEP 13083-100 Campinas, Sao Paulo Brazil
                [13 ]ISNI 0000 0001 2168 1229, GRID grid.9224.d, Department of Genetics, Faculty of Biology, , University of Seville, ; Avda de Reina Mercedes 6, 41012 Sevilla, Spain
                [14 ]ISNI 0000 0001 2298 5320, GRID grid.5173.0, Fungal Genetics and Genomics Unit, Department of Applied Genetics and Cell Biology, , University of Natural Resources and Life Sciences (BOKU) Vienna, ; Vienna, Austria
                [15 ]GRID grid.66859.34, , Broad Institute of Harvard and MIT, ; 75 Ames St, Cambridge, MA 02142 USA
                [16 ]ISNI 0000 0004 1790 4137, GRID grid.35155.37, College of Food Science and Technology, , Huazhong Agricultural University, ; Wuhan, 430070 China
                [17 ]ISNI 0000 0001 0723 2494, GRID grid.411087.b, Department of Biochemistry and Tissue Biology, , Institute of Biology, University of Campinas, ; CEP 13083-862 Campinas, SP Brazil
                [18 ]ISNI 0000 0001 1088 8582, GRID grid.7122.6, Department of Biotechnology and Microbiology, Faculty of Science and Technology, , University of Debrecen, ; Egyetem tér 1, 4032 Debrecen, Hungary
                [19 ]Institute of Sciences of Food Production (ISPA), National Research Council (CNR), via Provinciale Lecce-Monteroni, 73100 Lecce, Italy
                [20 ]Institute of Biosciences and Applications, Microbial Molecular Genetics Laboratory, National Center for Scientific Research, Demokritos (NCSRD), Athens, Greece
                [21 ]ISNI 0000 0004 1936 8868, GRID grid.4563.4, School of Life Sciences, , University of Nottingham, ; University Park, Nottingham, NG7 2RD UK
                [22 ]ISNI 0000 0001 2176 4817, GRID grid.5399.6, , CNRS, Aix-Marseille Université, ; Marseille, France
                [23 ]GRID grid.418532.9, , Institut Pasteur de Montevideo, Unidad Mixta INIA-IPMont, ; Mataojo 2020, CP11400 Montevideo, Uruguay
                [24 ]INRA, USC 1408 AFMB, 13288 Marseille, France
                [25 ]ISNI 0000 0001 0619 1117, GRID grid.412125.1, Department of Biological Sciences, , King Abdulaziz University, ; Jeddah, Saudi Arabia
                [26 ]ISNI 0000 0004 0410 2071, GRID grid.7737.4, Department of Food and Environmental Sciences, , University of Helsinki, ; Viikinkaari 9, Helsinki, Finland
                [27 ]Dutch DNA Biotech BV, Utrechtseweg 48, 3703AJ Zeist, The Netherlands
                [28 ]ISNI 0000000084992262, GRID grid.7177.6, , Swammerdam Institute for Life Sciences, University of Amsterdam, ; Amsterdam, The Netherlands
                [29 ]ISNI 0000 0001 0721 1626, GRID grid.11914.3c, School of Biology, , University of St Andrews, ; St Andrews, Fife KY16 9TH UK
                [30 ]ISNI 0000 0001 1088 8582, GRID grid.7122.6, Department of Medicine, Faculty of Medicine, , University of Debrecen, ; Nagyerdei krt. 98, 4032 Debrecen, Hungary
                [31 ]ISNI 0000 0001 0482 5331, GRID grid.411984.1, Department of Medical Informatics, , University Medical Centre, ; Robert-Koch-Str.40, 37075 Göttingen, Germany
                [32 ]ISNI 0000 0001 0482 5331, GRID grid.411984.1, Department of Molecular Biology, , Universitätsmedizin Göttingen, ; Humboldtallee 23, Göttingen, 37073 Germany
                [33 ]ISNI 0000 0001 2176 4817, GRID grid.5399.6, , INRA, Aix-Marseille Univ, BBF, Biodiversité et Biotechnologie Fongiques, ; Marseille, France
                [34 ]GRID grid.473653.0, , Institute of Sciences of Food Production (ISPA), National Research Council (CNR), ; Via Amendola 122/O, 70126 Bari, Italy
                [35 ]ISNI 0000 0001 1945 7738, GRID grid.419051.8, Departamento de Biotecnología, , Instituto de Agroquímica y Tecnología de Alimentos, Consejo Superior de Investigaciones Científicas (CSIC), ; Paterna, Valencia, Spain
                [36 ]ISNI 0000 0001 2163 588X, GRID grid.411247.5, Departamento de Genética e Evolução, , Centro de Ciências Biológicas e da Saúde, Universidade Federal de São Carlos, ; São Carlos, São Paulo Brazil
                [37 ]ISNI 0000 0000 8578 2742, GRID grid.6341.0, Uppsala BioCenter, Department of Microbiology, , Swedish University of Agricultural Sciences, ; P.O. Box 7025, 750 07 Uppsala, Sweden
                [38 ]ISNI 0000 0001 2292 8254, GRID grid.6734.6, Institute of Biotechnology, Department Applied and Molecular Microbiology, , Berlin University of Technology, ; Gustav-Meyer-Allee 25, 13355 Berlin, Germany
                [39 ]ISNI 0000 0001 1088 8582, GRID grid.7122.6, MTA-DE Momentum, Laboratory of Protein Dynamics, Department of Biochemistry and Molecular Biology, , University of Debrecen, ; Nagyerdei krt.98., 4032 Debrecen, Hungary
                [40 ]ISNI 0000 0001 0661 1556, GRID grid.258803.4, , School of Food Science and Biotechnology, Kyungpook National University, ; Daegu, 702-701 Republic of Korea
                [41 ]ISNI 0000000121657640, GRID grid.11630.35, Sección Bioquímica, Departamento de Biología Celular y Molecular, Facultad de Ciencias, , Universidad de la República, ; Montevideo, Uruguay
                [42 ]ISNI 0000 0001 0075 5874, GRID grid.7892.4, Department of Microbiology, , Karlsruhe Institute of Technology, Institute for Applied Biosciences, ; Hertzstrasse 16,, 76187 Karlsruhe, Germany
                [43 ]Department of Biology, School of Science, University of Sulaimani, Al Sulaymaneyah, Iraq
                [44 ]ISNI 0000 0001 1088 8582, GRID grid.7122.6, Institute of Food Science, Faculty of Agricultural and Food Sciences and Environmental Management, , University of Debrecen, ; 4032 Debrecen, Hungary
                [45 ]ISNI 0000 0001 0721 6013, GRID grid.8954.0, Department of Biology, Biotechnical Faculty, , University of Ljubljana, ; Jamnikarjeva 101, 1000 Ljubljana, Slovenia
                [46 ]ISNI 0000 0001 0143 807X, GRID grid.418398.f, , Systems Biology/Bioinformatics group, Leibniz Institute for Natural Product Research and Infection Biology, Hans Knoell Institute, (HKI), ; Beutenbergstr. 11a, 07745 Jena, Germany
                [47 ]ISNI 0000000419368956, GRID grid.168010.e, Department of Genetics, , Stanford University, ; Stanford, CA 94305-5120 USA
                [48 ]ISNI 0000 0001 0737 1259, GRID grid.36567.31, Department of Plant Pathology, , Kansas State University, ; Manhattan, KS 66506 USA
                [49 ]ISNI 0000 0004 1936 8630, GRID grid.410319.e, , Centre for Structural and Functional Genomics, Concordia University, ; 7141 Sherbrooke Street West, Montreal, QC H4B 1R6 Canada
                [50 ]ISNI 0000 0001 2181 8870, GRID grid.5170.3, Department of Biotechnology and Biomedicine, , Technical University of Denmark, ; Søltofts Plads 223, 2800 Kongens Lyngby, Denmark
                [51 ]ISNI 0000 0001 2167 3675, GRID grid.14003.36, Departments of Bacteriology and Genetics, , University of Wisconsin-Madison, ; 1550 Linden Drive, Madison, WI 53706 USA
                [52 ]Fungal Biotechnology Team, Pacific Northwest National Laboratory, Richland, Washington, 99352 USA
                [53 ]ISNI 0000 0001 1939 2794, GRID grid.9613.d, Department of Molecular and Applied Microbiology, , Leibniz-Institute for Natural Product Research and Infection Biology - Hans Knoell Institute (HKI) and Institute for Microbiology, Friedrich Schiller University Jena, ; Beutenbergstr. 11a, 07745 Jena, Germany
                [54 ]ISNI 0000 0004 1937 0722, GRID grid.11899.38, Faculdade de Ciências Farmacêuticas de Ribeirão Preto, , Universidade de São Paulo, ; Av. do Café S/N, CEP 14040-903 Ribeirão Preto, São Paulo Brazil
                [55 ]ISNI 0000 0001 2106 0692, GRID grid.266515.3, Department of Molecular Biosciences, , University of Kansas, ; Lawrence, Kansas 66045 USA
                [56 ]ISNI 0000 0001 2113 8111, GRID grid.7445.2, Department of Microbiology, , Imperial College, ; London, SW7 2AZ UK
                [57 ]Institute for Integrative Biology of the Cell (I2BC), CEA, CNRS, University Paris‐Sud, Université Paris‐Saclay, 91198 Gif‐sur‐Yvette cedex, France
                [58 ]ISNI 0000 0001 2348 4034, GRID grid.5329.d, Research Division Biochemical Technology, , Institute of Chemical Engineering, TU Wien, ; Gumpendorferstraße 1a, 1060 Vienna, Austria
                [59 ]GRID grid.66859.34, , Broad Institute, ; 415 Main St, Cambridge, MA 02142 USA
                [60 ]Present address: VTT Brasil, Alameda Inajá, 123, CEP 06460-055 Barueri, São Paulo Brazil
                [61 ]GRID grid.431777.1, , Present address: CSIRO Publishing, ; Unipark, Building 1 Level 1, 195 Wellington Road, Clayton, VIC 3168 Australia
                [62 ]Present address: Université Libre de Bruxelles Institute of Molecular Biology and Medicine (IBMM), Brussels, Belgium
                [63 ]Present address: Instituto de Profesores Artigas, Consejo de Formación en Educación, ANEP, CP 11800, Av. del Libertador 2025, Montevideo, Uruguay
                [64 ]ISNI 0000 0001 2108 7481, GRID grid.9594.1, Present Address: Department of Chemistry, , University of Ioannina, ; Ioannina, 45110 Greece
                [65 ]ISNI 0000 0001 2289 6897, GRID grid.15447.33, , Present address: Center for Algorithmic Biotechnology, St.Petersburg State University, ; St. Petersburg, Russia
                [66 ]ISNI 0000 0001 0407 1584, GRID grid.414336.7, , Present address: Aix-Marseille Université, Unité de Recherche sur les Maladies Infectieuses et Tropicales Emergentes (URMITE), UM63, CNRS 7278, IRD 198, INSERM U1095, IHU Méditerranée Infection, Pôle des Maladies Infectieuses, Assistance Publique-Hôpitaux de Marseille, Faculté de Médecine, ; 27 Bd Jean Moulin, 13005 Marseille, France
                [67 ]ISNI 0000 0001 1523 2072, GRID grid.437386.d, , Present address: Swedish Chemicals Agency, ; Box 2, 172 13 Sundbyberg, Sweden
                [68 ]Present address: Instituto de Ciencia y Tecnología Dr. César Milstein, Fundación Pablo Cassará, CONICET, Saladillo 2468 C1440FFX, Ciudad de Buenos Aires, Argentina
                [69 ]ISNI 0000 0004 1936 8630, GRID grid.410319.e, , Present address: Centre for Structural and Functional Genomics, Concordia University, ; 7141 Sherbrooke Street West, Montreal, QC H4B 1R6 Canada
                [70 ]Present address: INRA UMR1198 Biologie du Développement et de la Reproduction - Domaine de Vilvert, Jouy en Josas, 78352 Cedex France
                [71 ]ISNI 0000 0001 2292 8254, GRID grid.6734.6, Present address: Department Applied and Molecular Microbiology, , Institute of Biotechnology, Berlin University of Technology, ; Gustav-Meyer-Allee 25, 13355 Berlin, Germany
                [72 ]Present address: BaseClear B.V., Einsteinweg 5, 2333 CC Leiden, The Netherlands
                [73 ]Present address: Seres Therapeutics, 200 Sidney St, Cambridge, MA 02139 USA
                [74 ]ISNI 0000 0004 1936 8630, GRID grid.410319.e, , Present address: Centre of Functional and Structure Genomics Biology Department Concordia University, ; 7141 Sherbrooke St. W., Montreal, QC H4B 1R6 Canada
                Article
                1151
                10.1186/s13059-017-1151-0
                5307856
                28196534
                70171b8b-54bd-4957-a35b-16e82ae0f98c
                © The Author(s). 2017

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 5 July 2016
                : 10 January 2017
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100003549, Országos Tudományos Kutatási Alapprogramok;
                Award ID: K100464
                Award ID: NN116519
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100002347, Bundesministerium für Bildung und Forschung;
                Funded by: FundRef http://dx.doi.org/10.13039/501100001659, Deutsche Forschungsgemeinschaft;
                Award ID: FOR1334/2
                Award ID: FOR1334/2
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100001809, National Natural Science Foundation of China;
                Award ID: 31330059
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100002338, Ministry of Education of the People's Republic of China;
                Award ID: 2662014BQ051
                Award ID: 2662015QC003
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100003958, Stichting voor de Technische Wetenschappen;
                Award ID: UGC 14270
                Award ID: LGC 7393
                Award Recipient :
                Funded by: Austrian Science Fund (AT)
                Award ID: M01693-B22
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100004085, Ministry of Education, Science and Technology ;
                Award ID: 2011-0031955
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100001602, Science Foundation Ireland;
                Award ID: 13/CDA/2142
                Award Recipient :
                Funded by: Kurdistan Regional Government of Iraq
                Funded by: FundRef http://dx.doi.org/10.13039/100009689, British Mycological Society;
                Funded by: FundRef http://dx.doi.org/10.13039/501100000268, Biotechnology and Biological Sciences Research Council;
                Funded by: FundRef http://dx.doi.org/10.13039/100004322, Agilent Technologies;
                Award ID: #2871
                Funded by: Novo Nordisk Foundation
                Award ID: 13OC0005201
                Funded by: MINECO/FEDER
                Award ID: AGL2011-29925
                Award ID: AGL2015-66131- AGL2015-66131-C2-2-R
                Award Recipient :
                Funded by: Irving S. Johnson fund
                Funded by: FundRef http://dx.doi.org/10.13039/501100001807, Fundação de Amparo à Pesquisa do Estado de São Paulo;
                Award ID: 2012/19040-0
                Award ID: 2014/10351-8
                Award Recipient :
                Funded by: CNPq
                Award ID: 442333/2014-5
                Award ID: 441912/2014-1
                Award Recipient :
                Funded by: Dirección General de Apoyo al Personal Académico
                Award ID: IN 225710
                Award ID: IN219813
                Award Recipient :
                Funded by: Slovenian Research Agency
                Award ID: P1-0391
                Award ID: J4-7162
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100003621, Ministry of Science, ICT and Future Planning;
                Award ID: 2011-0031955
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000015, U.S. Department of Energy;
                Award ID: DE-AC02-05CH11231
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100008398, Villum Fonden;
                Award ID: VKR023437
                Award ID: VKR023437
                Funded by: FundRef http://dx.doi.org/10.13039/501100004285, Saint Petersburg State University;
                Award ID: 15.61.951.2015
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100001807, Fundação de Amparo à Pesquisa do Estado de São Paulo;
                Funded by: FundRef http://dx.doi.org/10.13039/501100003593, Conselho Nacional de Desenvolvimento Científico e Tecnológico;
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                Research
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                © The Author(s) 2017

                Genetics
                aspergillus,genome sequencing,comparative genomics,fungal biology
                Genetics
                aspergillus, genome sequencing, comparative genomics, fungal biology

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