Comparative "Omics" of the Fusarium fujikuroi Species Complex Highlights Differences in Genetic Potential and Metabolite Synthesis

. 2016 Dec 31 ; 8 (11) : 3574-3599. [epub] 20161231

Jazyk angličtina Země Velká Británie, Anglie Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid28040774

Species of the Fusarium fujikuroi species complex (FFC) cause a wide spectrum of often devastating diseases on diverse agricultural crops, including coffee, fig, mango, maize, rice, and sugarcane. Although species within the FFC are difficult to distinguish by morphology, and their genes often share 90% sequence similarity, they can differ in host plant specificity and life style. FFC species can also produce structurally diverse secondary metabolites (SMs), including the mycotoxins fumonisins, fusarins, fusaric acid, and beauvericin, and the phytohormones gibberellins, auxins, and cytokinins. The spectrum of SMs produced can differ among closely related species, suggesting that SMs might be determinants of host specificity. To date, genomes of only a limited number of FFC species have been sequenced. Here, we provide draft genome sequences of three more members of the FFC: a single isolate of F. mangiferae, the cause of mango malformation, and two isolates of F. proliferatum, one a pathogen of maize and the other an orchid endophyte. We compared these genomes to publicly available genome sequences of three other FFC species. The comparisons revealed species-specific and isolate-specific differences in the composition and expression (in vitro and in planta) of genes involved in SM production including those for phytohormome biosynthesis. Such differences have the potential to impact host specificity and, as in the case of F. proliferatum, the pathogenic versus endophytic life style.

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Abrusán G, Grundmann N, Demester L, Makalowski W. 2009. TEclass—a tool for automated classification of unknown eukaryotic transposable elements. Bioinformatics 25:1329–1330. PubMed

Aguileta G, et al. 2008. Assessing the performance of single-copy genes for recovering robust phylogenies. Syst Biol. 57:613–627. PubMed

Akagi Y, Akamatsu H, Otani H, Kodama M. 2009. Horizontal chromosome transfer, a mechanism for the evolution and differentiation of a plant-pathogenic fungus. Eukaryot Cell 8:1732–1738. PubMed PMC

Baer P, et al. 2014. Induced-fit mechanism in class I terpene cyclases. Angew Chem Int Ed Engl. 53:7652–7656. PubMed

Bai G, Shaner G. 1996. Variation in

Bajguz A, Piotrowska A. 2009. Conjugates of auxin and cytokinin. Phytochemistry 70:957–969. PubMed

Bendtsen JD, Jensen LJ, Blom N, Von Heijne G, Brunak S. 2004. Feature-based prediction of non-classical and leaderless protein secretion. Protein Eng Des Sel. 17:349–356. PubMed

Benson G. 1999. Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res. 27:573–580. PubMed PMC

Boetzer M, Henkel CV, Jansen HJ, Butler D, Pirovano W. 2011. Scaffolding pre-assembled contigs using SSPACE. Bioinformatics 27:578–579. PubMed

Bömke C, Tudzynski B. 2009. Diversity, regulation, and evolution of the gibberellin biosynthetic pathway in fungi compared to plants and bacteria. Phytochemistry 70:1876–1893. PubMed

Brakhage AA. 2013. Regulation of fungal secondary metabolism. Nat Rev Microbiol. 11:21–32. PubMed

Britz H, et al. 2002. Two new species of PubMed

Brock NL, Huss K, Tudzynski B, Dickschat JS. 2013. Genetic dissection of sesquiterpene biosynthesis by PubMed

Brock NL, Tudzynski B, Dickschat JS. 2011. Biosynthesis of sesqui- and diterpenes by the gibberellin producer PubMed

Brown DW, Butchko RA, Baker SE, Proctor RH. 2012a. Phylogenomic and functional domain analysis of polyketide synthases in PubMed

Brown DW, Butchko RA, Busman M, Proctor RH. 2012b. Identification of gene clusters associated with fusaric acid, fusarin, and perithecial pigment production in PubMed

Brown DW, et al. 2015. Identification of a 12-gene fusaric acid biosynthetic gene cluster in PubMed

Brown DW, Proctor RH. 2016. Insights into natural products biosynthesis from analysis of 490 polyketide synthases from PubMed

Brown DW, Proctor RH. 2013. Diversity of polyketide synthases in

Burkhardt I, et al. 2016. Mechanistic characterization of two sesquiterpene cyclases from the plant pathogen PubMed

Bushley KE, Turgeon BG. 2010. Phylogenomics reveals subfamilies of fungal nonribosomal peptide synthetases and their evolutionary relationships. BMC Evol Biol. 10:26. PubMed PMC

Chanclud E, et al. 2016. Cytokinin production by the rice blast fungus is a pivotal requirement for full virulence. PLoS Pathog. 12:e1005457.. PubMed PMC

Chiara M, et al. 2015. Genome sequencing of multiple isolates highlights subtelomeric genomic diversity within PubMed PMC

Citron CA, Rabe P, Dickschat JS. 2012. The scent of bacteria: headspace analysis for the discovery of natural products. J Nat Prod. 75:1765–1776. PubMed

Coleman JJ, et al. 2009. The genome of PubMed PMC

Colot HV, et al. 2006. A high-throughput gene knockout procedure for PubMed PMC

Crawford JM, Vagstad AL, Ehrlich KC, Townsend CA. 2008. Starter unit specificity directs genome mining of polyketide synthase pathways in fungi. Bioorg Chem. 36:16–22. PubMed PMC

Cuomo CA, et al. 2007. The PubMed

Darken MA, Jensen AL, Shu P. 1959. Production of gibberellic acid by fermentation. Appl Microbiol. 7:301–303. PubMed PMC

Desjardins AE. 2006. Fusarium mycotoxins: chemistry, genetics, and biology. St. Paul (MN): American Phytopathological Society (APS) Press.

Dickschat JS. 2015. Bacterial terpene cyclases. Nat Prod Rep. 33:87–110. PubMed

Ditengou FA, et al. 2015. Volatile signalling by sesquiterpenes from ectomycorrhizal fungi reprogrammes root architecture. Nat Commun. 6:6279. PubMed PMC

Donlin MJ. 2009. Using the Generic Genome Browser (GBrowse). Curr Protoc Bioinformatics Chapter 9: Unit 9.9. PubMed

Edgar R, Domrachev M, Lash AE. 2002. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 30:207–210. PubMed PMC

Edgar RC. 2004. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5:1.. PubMed PMC

Emanuelsson O, Nielsen H, Brunak S, von Heijne G. 2000. Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol. 300:1005–1016. PubMed

Freeman S, Shtienberg D, Maymon M, Levin AG, Ploetz RC. 2014. New insights into mango malformation disease epidemiology lead to a new integrated management strategy for subtropical environments. Plant Dis. 98:1456–1466. PubMed

Frisvad JC, Smedsgaard J, Samson RA, Larsen TO, Thrane U. 2007. Fumonisin B2 production by PubMed

Gardiner DM, et al. 2012. Comparative pathogenomics reveals horizontally acquired novel virulence genes in fungi infecting cereal hosts. PLoS Pathog. 8:e1002952.. PubMed PMC

Gawehns F, et al. 2014. The PubMed

Geiser DM, et al. 2013. One fungus, one name: defining the genus PubMed

Gnerre S, et al. 2011. High-quality draft assemblies of mammalian genomes from massively parallel sequence data. Proc Natl Acad Sci U S A. 108:1513–1518. PubMed PMC

Gohari AM, et al. 2015. Effector discovery in the fungal wheat pathogen PubMed PMC

Gordon SA, Weber RP. 1951. Colorimetric estimation of indoleacetic acid. Plant Physiol. 26:192–195. PubMed PMC

Grabherr MG, et al. 2011. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol. 29:644–652. PubMed PMC

Guindon S, et al. 2010. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol. 59:307–321. PubMed

Hansen FT, et al. 2015. An update to polyketide synthase and non-ribosomal synthetase genes and nomenclature in PubMed

Hinsch J, Galuszka P, Tudzynski P. 2016. Functional characterization of the first filamentous fungal tRNA‐isopentenyltransferase and its role in the virulence of PubMed

Hinsch J, et al. 2015. De novo biosynthesis of cytokinins in the biotrophic fungus PubMed

Hoffmeister D, Keller NP. 2007. Natural products of filamentous fungi: enzymes, genes, and their regulation. Nat Prod Rep. 24:393–416. PubMed

Jin JM, et al. 2010. Functional characterization and manipulation of the apicidin biosynthetic pathway in PubMed

Jurka J, et al. 2005. Repbase Update, a database of eukaryotic repetitive elements. Cytogenet Genome Res. 110:462–467. PubMed

Kasahara H. 2016. Current aspects of auxin biosynthesis in plants. Biosci Biotechnol Biochem. 80:34–42. PubMed

Khaldi N, Wolfe KH. 2011. Evolutionary origins of the fumonisin secondary metabolite gene cluster in PubMed PMC

Kim D, et al. 2013. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 14:R36.. PubMed PMC

Krogh A, Larsson B, von Heijne G, Sonnhammer EL. 2001. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol. 305:567–580. PubMed

Le SQ, Gascuel O. 2008. An improved general amino acid replacement matrix. Mol Biol Evol. 25:1307–1320. PubMed

Leslie JF, Summerell BA. 2006. The Fusarium laboratory manual, Oxford, UK: Blackwell Publishing.

Li R, et al. 2009. SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 25:1966–1967. PubMed

Lo Presti L, et al. 2015. Fungal effectors and plant susceptibility. Annu Rev Plant Biol. 66:513–545. PubMed

López‐Berges, et al. 2013. The velvet complex governs mycotoxin production and virulence of Fusarium oxysporum on plant and mammalian hosts. Mol Microbiol. 87:49–65. PubMed

Lowe TM, Eddy SR. 1997. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 25:955–964. PubMed PMC

Lysøe E, et al. 2014. The genome of the generalist plant pathogen PubMed PMC

Ma LJ, et al. 2013. PubMed

Ma LJ, et al. 2010. Comparative genomics reveals mobile pathogenicity chromosomes in PubMed PMC

Maor R, Haskin S, Levi-Kedmi H, Sharon A. 2004. In planta production of indole-3-acetic acid by PubMed PMC

Marasas WF, et al. 2004. Fumonisins disrupt sphingolipid metabolism, folate transport, and neural tube development in embryo culture and in vivo: a potential risk factor for human neural tube defects among populations consuming fumonisin-contaminated maize. J Nutr. 134:711–716. PubMed

Mashiguchi K, et al. 2011. The main auxin biosynthesis pathway in PubMed PMC

Morgavi DP, Riley RT. 2007. An historical overview of field disease outbreaks known or suspected to be caused by consumption of feeds contaminated with

Munawar A, Marshall JW, Cox RJ, Bailey AM, Lazarus CM. 2013. Isolation and characterisation of a ferrirhodin synthetase gene from the sugarcane pathogen PubMed

Munkvold G, Stahr HM, Logrieco A, Moretti A, Ritieni A. 1998. Occurrence of fusaproliferin and beauvericin in PubMed PMC

Niehaus E-M, et al. 2014a. Apicidin F: characterization and genetic manipulation of a new secondary metabolite gene cluster in the rice pathogen PubMed PMC

Niehaus E-M, et al. 2014b. Characterization of the fusaric acid gene cluster in PubMed

Niehaus E-M, et al. 2016. Sound of silence: the beauvericin cluster in PubMed

O'Donnell K, Cigelnik E, Nirenberg HI. 1998a. Molecular systematics and phylogeography of the

O'Donnell K, Kistler HC, Cigelnik E, Ploetz RC. 1998b. Multiple evolutionary origins of the fungus causing Panama disease of banana: concordant evidence from nuclear and mitochondrial gene genealogies. Proc Natl Acad Sci U S A. 95:2044–2049. PubMed PMC

O'Donnell K, et al. 2013. Phylogenetic analyses of RPB1 and RPB2 support a middle Cretaceous origin for a clade comprising all agriculturally and medically important fusaria. Fungal Genet Biol. 52:20–31. PubMed

Oide S, Berthiller F, Wiesenberger G, Adam G, Turgeon BG. 2015. Individual and combined roles of malonichrome, ferricrocin, and TAFC siderophores in PubMed PMC

Oren L, Ezrati S, Cohen D, Sharon A. 2003. Early events in the PubMed PMC

Parra G, Bradnam K, Ning Z, Keane T, Korf I. 2009. Assessing the gene space in draft genomes. Nucleic Acids Res. 37:289–297. PubMed PMC

Petersen TN, Brunak S, von Heijne G, Nielsen H. 2011. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8:785–786. PubMed

Pfaffl MW. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29:e45.. PubMed PMC

Ploetz RC, Freeman S. 2009. Foliar, floral and soilborne diseases, Chapter 8 In: Mukherjee SK, Litz RE, editors. The Mango: Botany, Production and Uses. Bodmin, UK: MPG Books Group; p. 231.

Price AL, Jones NC, Pevzner PA. 2005. PubMed

Proctor RH, Desjardins AE, Moretti A. 2009. Biological and chemical complexity of

Proctor RH, et al. 2013. Birth, death and horizontal transfer of the fumonisin biosynthetic gene cluster during the evolutionary diversification of PubMed

Rep M, Kistler HC. 2010. The genomic organization of plant pathogenicity in PubMed

Rösler SM, Sieber CMK, Humpf H-U, Tudzynski B. 2016. Interplay between pathway-specific and global regulation of the fumonisin gene cluster in the rice pathogen PubMed

Salamov AA, Solovyev VV. 2000. Ab initio gene finding in PubMed PMC

Schumacher J. 2012. Tools for PubMed

Sieber CMK, et al. 2014. The PubMed PMC

Slater GS, Birney E. 2005. Automated generation of heuristics for biological sequence comparison. BMC Bioinformatics 6:31.. PubMed PMC

Smit AFA, Hubley R, Green P. 1996. RepeatMasker Open-3.0. Seattle (WA: ): Institute for Systems Biology.

Stanke M, et al. 2006. AUGUSTUS: ab initio prediction of alternative transcripts. Nucleic Acids Res. 34:W435–W439. PubMed PMC

Studt L, et al. 2016. Two separate key enzymes and two pathway‐specific transcription factors are involved in fusaric acid biosynthesis in PubMed

Studt L, Wiemann P, Kleigrewe K, Humpf H-U, Tudzynski B. 2012. Biosynthesis of fusarubins accounts for pigmentation of PubMed PMC

Talavera G, Castresana J. 2007. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol. 56:564–577. PubMed

Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol. 30:2725–2729. PubMed PMC

Tamura T, Akutsu T. 2007. Subcellular location prediction of proteins using support vector machines with alignment of block sequences utilizing amino acid composition. BMC Bioinformatics 8:466.. PubMed PMC

Ter-Hovhannisyan V, Lomsadze A, Chernoff YO, Borodovsky M. 2008. Gene prediction in novel fungal genomes using an ab initio algorithm with unsupervised training. Genome Res. 18:1979–1990. PubMed PMC

Trapnell C, Pachter L, Salzberg SL. 2009. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25:1105–1111. PubMed PMC

Trapnell C, et al. 2012. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc. 7:562–578. PubMed PMC

Troncoso C, et al. 2010. Gibberellin biosynthesis and gibberellin oxidase activities in PubMed

Tsavkelova EA, et al. 2003a. Fungi associated with orchid roots in greenhouse conditions. Mikologiia I Fitopatologiia 37:57–63.

Tsavkelova EA, Lobakova ES, Kolomeitseva GL, Cherdyntseva TA, Netrusov AI. 2003b. Localization of associative cyanobacteria on the roots of epiphytic orchids. Microbiology 72:86–91. PubMed

Tsavkelova EA, et al. 2012. Identification and functional characterization of indole-3-acetamide-mediated IAA biosynthesis in plant-associated PubMed

Tudzynski B, Homann V, Feng B, Marzluf GA. 1999. Isolation, characterization and disruption of the PubMed

Tudzynski B, Sharon A. 2002. Biosynthesis, biological role and application of fungal phytohormones In:Osiewacz HD, editor. Industrial applications. Berlin: Springer; pp. 183–211.

Urbanova T, Tarkowska D, Novak O, Hedden P, Strnad M. 2013. Analysis of gibberellins as free acids by ultra performance liquid chromatography-tandem mass spectrometry. Talanta 112:85–94. PubMed

Vergara IA, Chen N. 2009. Using OrthoCluster for the detection of synteny blocks among multiple genomes. Curr Protoc Bioinformatics Chapter 6: Unit 6.10 6.10.1–18. PubMed

von Bargen KW, et al. 2015. Isolation and structure elucidation of fujikurins A-D: products of the PKS19 gene cluster in PubMed

Walter MC, et al. 2009. PEDANT covers all complete RefSeq genomes. Nucleic Acids Res. 37:D408–D411. PubMed PMC

Wiemann P, et al. 2012. The Sfp-type 4'-phosphopantetheinyl transferase Ppt1 of PubMed PMC

Wiemann P, et al. 2013. Deciphering the cryptic genome: genome-wide analyses of the rice pathogen PubMed PMC

Wight WD, Kim KH, Lawrence CB, Walton JD. 2009. Biosynthesis and role in virulence of the histone deacetylase inhibitor depudecin from PubMed

Williams AH, et al. 2016. Comparative genomics and prediction of conditionally dispensable sequences in legume–infecting Fusarium oxysporum formae speciales facilitates identification of candidate effectors. BMC Genomics 17:1.. PubMed PMC

Wingfield BD, et al. 2012. First fungal genome sequence from Africa: a preliminary analysis. S Afr J Sci. 108:01–09.

Wingfield MJ, et al. 2008. Pitch canker caused by

Wong P, et al. 2011. FGDB: revisiting the genome annotation of the plant pathogen PubMed PMC

Wootton JC, Federhen S. 1996. Analysis of compositionally biased regions in sequence databases. Meth Enzymol. 266:554–571. PubMed

Wu F. 2007. Measuring the economic impacts of

Xu JR, Leslie JF. 1996. A genetic map of Gibberella fujikuroi mating population A ( PubMed PMC

Xu Y, et al. 2008. Biosynthesis of the cyclooligomer depsipeptide beauvericin, a virulence factor of the entomopathogenic fungus PubMed

Yu C, Zavaljevski N, Desai V, Reifman J. 2011. QuartetS: a fast and accurate algorithm for large-scale orthology detection. Nucleic Acids Res. 39:e88.. PubMed PMC

Zeng X, et al. 2008. OrthoCluster: a new tool for mining synteny blocks and applications in comparative genomics. 11th International Conference on Extending Technology (EDBT), March 25–30, 2008, Nantes, France. pp. 656–667.

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