Genomic and transcriptomic analysis of the endophytic fungus Pestalotiopsis fici reveals its lifestyle and high potential for synthesis of natural products
详细信息    查看全文
  • 作者:Xiuna Wang (1) (2)
    Xiaoling Zhang (1)
    Ling Liu (1)
    Meichun Xiang (1)
    Wenzhao Wang (1)
    Xiang Sun (1)
    Yongsheng Che (3)
    Liangdong Guo (1)
    Gang Liu (1)
    Liyun Guo (2)
    Chengshu Wang (4)
    Wen-Bing Yin (1)
    Marc Stadler (5)
    Xinyu Zhang (1)
    Xingzhong Liu (1)

    1. State Key Laboratory of Mycology
    ; Institute of Microbiology ; Chinese Academy of Sciences ; Beijing ; China
    2. Department of Plant Pathology
    ; China Agricultural University ; Beijing ; China
    3. Department of Natural Products Chemistry
    ; Beijing Institute of Pharmacology & Toxicology ; Beijing ; China
    4. Key Laboratory of Insect Development and Evolutionary Biology
    ; Institute of Plant Physiology and Ecology ; Shanghai Institutes for Biological Sciences ; Chinese Academy of Sciences ; Shanghai ; China
    5. Department Microbial Drugs
    ; Helmholtz Centre for Infection Research ; Braunschweig ; Germany
  • 关键词:Genome ; Endophyte ; Pestalotiopsis fici ; Secondary metabolite
  • 刊名:BMC Genomics
  • 出版年:2015
  • 出版时间:December 2015
  • 年:2015
  • 卷:16
  • 期:1
  • 全文大小:3,852 KB
  • 参考文献:1. Stone JK, Bacon CW, White J. An overview of endophytic microbes: endophytism defined. In: Bacon CW, White JF, editors. Microbial endophytes. New York: Marcel Decker Inc; 2000. p. 29鈥?3.
    2. Rodriguez RJ, White JF, Arnold AE, Redman RS. Fungal endophytes: diversity and functional roles. New Phytol. 2009;182:314鈥?0. CrossRef
    3. Jalgaonwala RE, Mohite BV, Mahajan RT. A review: natural products from plant associated endophytic fungi. J Microbiol Biotechnol Res. 2011;1:21鈥?2.
    4. Strobel G, Daisy B, Castillo U, Harper J. Natural products from endophytic microorganisms. J Nat Prod. 2004;67:257鈥?8. CrossRef
    5. Schulz B, Boyle C, Draeger S, R枚mmert A-K, Krohn K. Endophytic fungi: a source of novel biologically active secondary metabolites. Mycol Res. 2002;106:996鈥?004. CrossRef
    6. Aly AH, Debbab A, Kjer J, Proksch P. Fungal endophytes from higher plants: a prolific source of phytochemicals and other bioactive natural products. Fungal Divers. 2010;41:1鈥?6. CrossRef
    7. Strobel G, Daisy B. Bioprospecting for microbial endophytes and their natural products. Microbiol Mol Biol R. 2003;67:491鈥?02. CrossRef
    8. Stierle A, Strobel G, Stierle D. Taxol and taxane production by / Taxomyces andreanae, an endophytic fungus of Pacific yew. Science. 1993;260:214鈥?. CrossRef
    9. Suryanarayanan TS, Thirunavukkarasu N, Govindarajulu MB, Gopalan V. Fungal endophytes: an untapped source of biocatalysts. Fungal Divers. 2012;54:19鈥?0. CrossRef
    10. Maharachchikumbura SSN, Guo LD, Chukeatirote E, Bahkali AH, Hyde KD. / Pestalotiopsis 鈥?morphology, phylogeny, biochemistry and diversity. Fungal Divers. 2011;50:167鈥?7. CrossRef
    11. Strobel G, Yang X, Sears J, Kramer R, Sidhu RS, Hess W. Taxol from / Pestalotiopsis microspora, an endophytic fungus of / Taxus wallachiana. Microbiology. 1996;142:435鈥?0. CrossRef
    12. Tejesvi M, Tamhankar S, Kini K, Rao V, Prakash H. Phylogenetic analysis of endophytic / Pestalotiopsis species from ethnopharmaceutically important medicinal trees. Fungal Divers. 2009;38:167鈥?3.
    13. Wei JG, Xu T, Guo LD, Liu AR, Zhang Y, Pan XH. Endophytic / Pestalotiopsis species associated with plants of / Podocarpaceae, / Theaceae and / Taxaceae in southern China. Fungal Divers. 2007;24:55鈥?4.
    14. Xu J, Ebada SS, Proksch P. / Pestalotiopsis a highly creative genus: chemistry and bioactivity of secondary metabolites. Fungal Divers. 2010;44:15鈥?1. CrossRef
    15. Yang XL, Zhang JZ, Luo DQ. The taxonomy, biology and chemistry of the fungal / Pestalotiopsis genus. Nat Prod Rep. 2012;29:622鈥?1. CrossRef
    16. Agarwal GP. Fungi causing plant diseases at Jabalpur (Madhya Pradesh)-III. J Indian Botanic. 1961;40:404鈥?.
    17. Liu L. Bioactive metabolites from the plant endophyte / Pestalotiopsis fici. Mycology. 2011;2:37鈥?5. CrossRef
    18. Liu L, Tian RR, Liu SC, Chen XL, Guo LD, Che YS. Pestaloficiols A鈥揈, bioactive cyclopropane derivatives from the plant endophytic fungus / Pestalotiopsis fici. Bioorg Med Chem. 2008;16:6021鈥?. CrossRef
    19. Liu L, Liu SC, Niu SB, Guo LD, Chen XL, Che YS. Isoprenylated chromone derivatives from the plant endophytic fungus / Pestalotiopsis fici. J Nat Prod. 2009;72:1482鈥?. CrossRef
    20. Liu SC, Guo LD, Che YS, Liu L. Pestaloficiols Q鈥揝 from the plant endophytic fungus / Pestalotiopsis fici. Fitoterapia. 2013;85:114鈥?. CrossRef
    21. Liu L, Liu SC, Chen XL, Guo LD, Che YS. Pestalofones A鈥揈, bioactive cyclohexanone derivatives from the plant endophytic fungus / Pestalotiopsis fici. Bioorg Med Chem. 2009;17:606鈥?3. CrossRef
    22. Liu SC, Ye X, Guo LD, Liu L. Cytotoxic isoprenylated epoxycyclohexanediols from the plant endophyte / Pestalotiopsis fici. Chin J Nat Med. 2011;9:374鈥?.
    23. Liu L, Liu SC, Jiang LH, Chen XL, Guo LD, Che YS. Chloropupukeananin, the first chlorinated pupukeanane derivative, and its precursors from / Pestalotiopsis fici. Org Lett. 2008;10:1397鈥?00. CrossRef
    24. Liu L, Li Y, Liu SC, Zheng ZH, Chen XL, Zhang H, et al. Chloropestolide A, an antitumor metabolite with an unprecedented spiroketal skeleton from / Pestalotiopsis fici. Org Lett. 2009;11:2836鈥?. CrossRef
    25. Liu L, Li Y, Li L, Cao Y, Guo LD, Liu G, et al. Spiroketals of / Pestalotiopsis fici provide evidence for a biosynthetic hypothesis involving diversified Diels鈥揂lder reaction cascades. J Org Chem. 2013;78:2992鈥?000. CrossRef
    26. Liu L, Niu SB, Lu XH, Chen XL, Zhang H, Guo LD, et al. Unique metabolites of / Pestalotiopsis fici suggest a biosynthetic hypothesis involving a Diels鈥揂lder reaction and thenmechanistic diversification. Chem Commun. 2010;46:460鈥?. CrossRef
    27. Liu L, Bruhn T, Guo LD, Gotz DCG, Brun R, Stich A, et al. Chloropupukeanolides C鈥揈: cytotoxic pupukeanane chlorides with a spiroketal skeleton from / Pestalotiopsis fici. Chem Eur J. 2011;17:2604鈥?3. CrossRef
    28. Keller NP, Turner G, Bennett JW. Fungal secondary metabolism 鈥?from biochemistry to genomics. Nat Rev Microbiol. 2005;3:937鈥?7. CrossRef
    29. Crawford JM, Clardy J. Microbial genome mining answers longstanding biosynthetic questions. Proc Natl Acad Sci U S A. 2012;109:7589鈥?0. CrossRef
    30. Sanchez JF, Somoza AD, Keller NP, Wang CC. Advances in / Aspergillus secondary metabolite research in the post-genomic era. Nat Prod Rep. 2012;29:351鈥?1. CrossRef
    31. Summerell BA, Laurence MH, Liew ECY, Leslie JF. Biogeography and phylogeography of Fusarium: a review. Fungal Divers. 2010;44:3鈥?3. CrossRef
    32. Veneault-Fourrey C, Martin F. Mutualistic interactions on a knife-edge between saprotrophy and pathogenesis. Curr Opin Plant Biol. 2011;14:444鈥?0. CrossRef
    33. Pao SS, Paulsen IT, Saier MH. Major facilitator superfamily. Microbiol Mol Biol R. 1998;62:1鈥?4.
    34. Reddy VS, Shlykov MA, Castillo R, Sun EI, Saier Jr MH. The major facilitator superfamily (MFS) revisited. FEBS J. 2012;279:2022鈥?5. CrossRef
    35. Fox EM, Howlett BJ. Secondary metabolism: regulation and role in fungal biology. Curr Opin Microbiol. 2008;11:481鈥?. CrossRef
    36. Dufour N, Rao RP. Secondary metabolites and other small molecules as intercellular pathogenic signals. FEMS Microbiol Lett. 2011;314:10鈥?. CrossRef
    37. Xu XX, Liu L, Zhang F, Wang WZ, Li JY, Guo LD, et al. Identification of the first diphenyl ether gene cluster for pestheic acid biosynthesis in plant endophyte / Pestalotiopsis fici. Chem Bio Chem. 2013;15:284鈥?2. CrossRef
    38. Kim HJ, Ruszczycky MW, Choi SH, Liu YN, Liu HW. Enzyme-catalysed [4+2] cycloaddition is a key step in the biosynthesis of spinosyn A. Nature. 2011;473:109鈥?2. CrossRef
    39. Ose T, Watanabe K, Mie T, Honma M, Watanabe H, Yao M, et al. Insight into a natural Diels-Alder reaction from the structure of macrophomate synthase. Nature. 2003;422:185鈥?. CrossRef
    40. Galagan JE, Calvo SE, Borkovich KA, Selker EU, Read ND, Jaffe D, et al. The genome sequence of the filamentous fungus / Neurospora crassa. Nature. 2003;422:859鈥?8. CrossRef
    41. Cuomo CA, G眉ldener U, Xu JR, Trail F, Turgeon BG, Di Pietro A, et al. The / Fusarium graminearum genome reveals a link between localized polymorphism and pathogen specialization. Science. 2007;317:1400鈥?. CrossRef
    42. Schulz B, R枚mmert AK, Dammann U, Aust HJ, Strack D. The endophyte-host interaction: a balanced antagonism? Mycol Res. 1999;103:1275鈥?3. CrossRef
    43. Kusari S, Hertweck C, Spiteller M. Chemical ecology of endophytic fungi: origins of secondary metabolites. Chem Biol. 2012;19:792鈥?. CrossRef
    44. Cresnar B, Petric S. Cytochrome P450 enzymes in the fungal kingdom. BBA-Proteins Proteom. 1814;2011:29鈥?5.
    45. Deng J, Carbone I, Dean RA. The evolutionary history of cytochrome P450 genes in four filamentous Ascomycetes. BMC Evol Biol. 2007;7:30. CrossRef
    46. Chen SL, Xu J, Liu C, Zhu YJ, Nelson DR, Zhou SG, et al. Genome sequence of the model medicinal mushroom / Ganoderma lucidum. Nat Commun. 2012;3:913. CrossRef
    47. Ohm RA, Feau N, Henrissat B, Schoch CL, Horwitz BA, Barry KW, et al. Diverse lifestyles and strategies of plant pathogenesis encoded in the genomes of eighteen / Dothideomycetes fungi. PLoS Pathog. 2012;8:e1003037. CrossRef
    48. Zhao ZT, Liu HQ, Wang CF, Xu J-R. Comparative analysis of fungal genomes reveals different plant cell wall degrading capacity in fungi. BMC Genomics. 2013;14:274. CrossRef
    49. Spanu PD, Abbott JC, Amselem J, Burgis TA, Soanes DM, St眉ber K, et al. Genome expansion and gene loss in powdery mildew fungi reveal tradeoffs in extreme parasitism. Science. 2010;330:1543鈥?. CrossRef
    50. Duplessis S, Cuomo CA, Lin Y-C, Aerts A, Tisserant E, Veneault-Fourrey C, et al. Obligate biotrophy features unraveled by the genomic analysis of rust fungi. Proc Natl Acad Sci U S A. 2011;108:9166鈥?1. CrossRef
    51. Martin F, Aerts A, Ahren D, Brun A, Danchin E, Duchaussoy F, et al. The genome of / Laccaria bicolor provides insights into mycorrhizal mymbiosis. Nature. 2008;452:88鈥?3. CrossRef
    52. Martin F, Kohler A, Murat C, Balestrini R, Coutinho PM, Jaillon O, et al. P茅rigord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis. Nature. 2010;464:1033鈥?. CrossRef
    53. Balestrini R, Sillo F, Kohler A, Schneider G, Faccio A, Tisserant E, et al. Genome-wide analysis of cell wall-related genes in / Tuber melanosporum. Curr Genet. 2012;58:165鈥?7. CrossRef
    54. Frank AC. The genomes of endophytic bacteria. In: Pirttil盲 AM, Frank AC, editors. Endophytes of forest trees. Heidelberg London New York: Springer Science + Business Media; 2011. p. 107鈥?6. CrossRef
    55. Lawrence DP, Kroken S, Pryor BM, Arnold AE. Interkingdom gene transfer of a hybrid NPS/PKS from bacteria to filamentous ascomycota. PLoS One. 2011;6:e28231. CrossRef
    56. Kroken S, Glass NL, Taylor JW, Yoder O, Turgeon BG. Phylogenomic analysis of type I polyketide synthase genes in pathogenic and saprobic ascomycetes. Proc Natl Acad Sci U S A. 2003;100:15670鈥?. CrossRef
    57. Haas BJ, Zeng QD, Pearson MD, Cuomo CA, Wortman JR. Approaches to fungal genome annotation. Mycology. 2011;2:118鈥?1.
    58. Ter-Hovhannisyan V, Lomsadze A, Chernoff YO, Borodovsky M. Gene prediction in novel fungal genomes using ab initio algorithm with unsupervised training. Genome Res. 2008;18:1979鈥?0. CrossRef
    59. GENEID. http://genome.crg.es/software/geneid/index.html.
    60. Solovyev V, Kosarev P, Seledsov I, Vorobyev D. Automatic annotation of eukaryotic genes, pseudogenes and promoters. Genome Biol. 2006;7 Suppl 1:S10. CrossRef
    61. Stanke M, Morgenstern B. AUGUSTUS: a web server for gene prediction in eukaryotes that allows user-defined constraints. Nucleic Acids Res. 2005;33:W465鈥?. CrossRef
    62. Majoros WH, Pertea M, Salzberg SL. TigrScan and GlimmerHMM: two open-source ab initio eukaryotic gene-finders. Bioinformatics. 2004;20:2878鈥?. CrossRef
    63. Birney E, Clamp M, Durbin R. GeneWise and GenomeWise. Genome Res. 2004;14:988鈥?5. CrossRef
    64. Bairoch A, Apweiler R, Wu CH, Barker WC, Boeckmann B, Ferro S, et al. The universal protein resource (UniProt). Nuclei Acids Res. 2005;33 Suppl 1:154鈥?.
    65. PASA. http://pasa.sourceforge.net/.
    66. Haas BJ, Salzberg SL, Zhu W, Pertea M, Allen JE, Orvis J, et al. Automated eukaryotic gene structure annotation using EVidenceModeler and the Program to Assemble Spliced Alignments. Genome Biol. 2008;9:R7. CrossRef
    67. Finn RD, Clements J, Eddy SR. HMMER web server: interactive sequence similarity searching. Nuclei Acids Res. 2011;39 Suppl 2:W29. CrossRef
    68. Finn RD, Tate J, Mistry J, Coggill PC, Sammut JS, Hotz HR, et al. The Pfam protein families database. Nuclei Acids Res. 2008;36 Suppl 1:D281鈥?.
    69. Haft DH, Selengut JD, White O. The TIGRFAMs database of protein families. Nucleic Acids Res. 2003;31:371鈥?. CrossRef
    70. Zdobnov EM, Apweiler R. InterProScan 鈥?an integration platform for the signature-recognition methods in InterPro. Bioinformatics. 2001;17:847鈥?. CrossRef
    71. Gene Ontology consortium. The gene ontology (GO) database and informatics resource. Nuclei Acids Res. 2004;32:D258鈥?1. CrossRef
    72. Ogata H, Goto S, Sato K, Fujibuchi W, Bono H, Kanehisa M. KEGG: Kyoto encyclopedia of genes and genomes. Nuclei Acids Res. 1999;27:29鈥?4. CrossRef
    73. Tatusov RL, Fedorova ND, Jackson JD, Jacobs AR, Kiryutin B, Koonin EV, et al. The COG database: an updated version includes eukaryotes. BMC Bioinformatics. 2003;4:41. CrossRef
    74. Ruepp A, Zollner A, Maier D, Albermam K, Hani J, Mokrejs M, et al. The FunCat, a functional annotation scheme for systematic classification of proteins from whole genomes. Nuclei Acids Res. 2008;32:5539鈥?5. CrossRef
    75. Li L, Stoeckert CJ, Roos DS. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res. 2003;13:2178鈥?9. CrossRef
    76. Price AL, Jones NC, Pevzner PA. / De novo identification of repeat families in large genomes. Bioinformatics. 2005;21 Suppl 1:351鈥?. CrossRef
    77. Jurka J, Kapitonov VV, Pavlicek A, Klonowski P, Kohany O, Walichiewicz J. Repbase Update, a database of eukaryotic repetitive elements. Cytogenet Genome Res. 2005;110:462鈥?. CrossRef
    78. Smit A, Green P. RepeatMasker. http://repeatmasker.org.
    79. Hane JK, Oliver RP. RIPCAL: a tool for alignment-based analysis of repeat-induced point mutations in fungal genomic sequences. BMC Bioinformatics. 2008;478:1478鈥?105.
    80. De Bie T, Cristianini N, Demuth JP, Hahn MW. CAFE: a computational tool for the study of gene family evolution. Bioinformatics. 2006;22:1269鈥?1. CrossRef
    81. Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics. 2006;22:2688鈥?0. CrossRef
    82. Sanderson MJ. r8s: inferring absolute rates of molecular evolution and divergence times in the absence of a molecular clock. Bioinformatics. 2003;19:301鈥?. CrossRef
    83. L眉cking R, Huhndorf S, Pfister DH, Plata ER, Lumbsch HT. Fungi evolved right on track. Mycologia. 2009;101:810鈥?2. CrossRef
    84. Yin YB, Mao XZ, Yang JC, Chen X, Mao FL, Xu Y. dbCAN: a web resource for automated carbohydrate-active enzyme annotation. Nuclei Acids Res. 2012;40(W1):445鈥?1. CrossRef
    85. R. http://www.r-project.org/.
    86. Khaldi N, Seifuddin FT, Turner G, Haft D, Nierman WC, Wolfe KH, et al. SMURF: genomic mapping of fungal secondary metabolite clusters. Fungal Genet Biol. 2010;47:736鈥?1. CrossRef
    87. Medema MH, Blin K, Cimermancic P, de Jager V, Zakrzewski P, Fischbach MA, et al. antiSMASH: rapid identification, annotation and analysis of secondary metabolite biosynthesis gene clusters in bacterial and fungal genome sequences. Nuclei Acids Res. 2011;39 Suppl 2:339鈥?6. CrossRef
    88. Ansari M, Yadav G, Gokhale RS, Mohanty D. NRPS-PKS: a knowledge-based resource for analysis of NRPS/PKS megasynthases. Nuclei Acids Res. 2004;32 Suppl 2:405鈥?3. CrossRef
    89. Lin SH, Yoshimoto M, Lyu PC, Tang CY, Arita M. Phylogenomic and domain analysis of iterative polyketide synthases in / Aspergillus species. Evol Bioinform. 2012;8:373鈥?7.
    90. Katoh K, Toh H. Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinform. 2008;9:286鈥?8. CrossRef
    91. Letunic I, Bork P. Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics. 2007;23:127鈥?. CrossRef
    92. Kasahara K, Miyamoto T, Fujimoto T, Oguri H, Tokiwano T, Oikawa H, et al. Solanapyrone synthase, a possible Diels-Alderase and iterative type I polyketide synthase encoded in a biosynthetic gene cluster from / Alternaria solani. ChemBioChem. 2010;11:1245鈥?2. CrossRef
    93. Brenner S, Johnson M, Bridgham J, Golda G, Lloyd DH, Johnson D, et al. Gene expression analysis by massively parallel signature sequencing (MPSS) on microbead arrays. Nat Biotechnol. 2000;18:630鈥?. CrossRef
    94. Trapnell C, Pachter L, Salzberg SL. Tophat: discovering splice junctions with RNA-Seq. Bioinformatics. 2009;25:1105鈥?1. CrossRef
    95. IGB-browser. http://bioviz.org/igb/index.html.
  • 刊物主题:Life Sciences, general; Microarrays; Proteomics; Animal Genetics and Genomics; Microbial Genetics and Genomics; Plant Genetics & Genomics;
  • 出版者:BioMed Central
  • ISSN:1471-2164
文摘
Background In recent years, the genus Pestalotiopsis is receiving increasing attention, not only because of its economic impact as a plant pathogen but also as a commonly isolated endophyte which is an important source of bioactive natural products. Pestalotiopsis fici Steyaert W106-1/CGMCC3.15140 as an endophyte of tea produces numerous novel secondary metabolites, including chloropupukeananin, a derivative of chlorinated pupukeanane that is first discovered in fungi. Some of them might be important as the drug leads for future pharmaceutics. Results Here, we report the genome sequence of the endophytic fungus of tea Pestalotiopsis fici W106-1/CGMCC3.15140. The abundant carbohydrate-active enzymes especially significantly expanding pectinases allow the fungus to utilize the limited intercellular nutrients within the host plants, suggesting adaptation of the fungus to endophytic lifestyle. The P. fici genome encodes a rich set of secondary metabolite synthesis genes, including 27 polyketide synthases (PKSs), 12 non-ribosomal peptide synthases (NRPSs), five dimethylallyl tryptophan synthases, four putative PKS-like enzymes, 15 putative NRPS-like enzymes, 15 terpenoid synthases, seven terpenoid cyclases, seven fatty-acid synthases, and five hybrids of PKS-NRPS. The majority of these core enzymes distributed into 74 secondary metabolite clusters. The putative Diels-Alderase genes have undergone expansion. Conclusion The significant expansion of pectinase encoding genes provides essential insight in the life strategy of endophytes, and richness of gene clusters for secondary metabolites reveals high potential of natural products of endophytic fungi.

© 2004-2018 中国地质图书馆版权所有 京ICP备05064691号 京公网安备11010802017129号

地址:北京市海淀区学院路29号 邮编:100083

电话:办公室:(+86 10)66554848;文献借阅、咨询服务、科技查新:66554700