Advertisement

Applied Microbiology and Biotechnology

, Volume 101, Issue 4, pp 1593–1604 | Cite as

Complete mitochondrial genome of the endophytic fungus Pestalotiopsis fici: features and evolution

  • Shu Zhang
  • Xiu-Na Wang
  • Xiao-Ling Zhang
  • Xing-Zhong Liu
  • Yong-Jie ZhangEmail author
Genomics, transcriptomics, proteomics

Abstract

Endophytic fungi (EF) live within plants and have profound impacts on plant communities. They are astonishingly diverse but poorly studied at the genome level. Herein, we assembled the mitochondrial genome (mitogenome) of the EF Pestalotiopsis fici, annotated and compared it with those of other relatives to better understand the evolution of the EF lineage. Except for standard fungal mitochondrial genes, the 69,529-bp circular mitogenome of P. fici harbors 18 introns acquired possibly through lateral transfer from other fungi and nine free-standing open reading frames with some scarcely seen in fungal mitogenomes. BLAST analysis detected no obvious duplication events of large fragments between mitochondrial and nuclear genomes of the fungus. Transcription analyses validated the expression of all mitochondrial genes, while most genes showed higher expression on rice than in two other media. The mitogenome of P. fici is highly syntenic with the Xylariales species Annulohypoxylon stygium and the endophyte Epichloe festucae var. lolii, but lacks synteny with another endophyte Penicillium polonicum. This study reports the first mitogenome of Pestalotiopsis and the third published mitogenome from an EF and provides insights into the evolution of the EF lineage.

Keywords

Pestalotiopsis fici Mitochondrial genome Endophyte Xylariales RNA-seq 

Notes

Acknowledgements

This study was funded by the National Science Foundation of China (81102759), the Natural Science Foundation of Shanxi Province (2014021030-2, 201601D011065), the Fund Program for the Scientific Activities of Selected Returned Overseas Professionals in Shanxi Province, and the Special Fund for Large Scientific Instruments and Equipments in Shanxi Province. The authors thank Xiaoqing Yang for her help in drawing the circular mitochondrial map.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

Ethical statement

This article does not contain any studies with human participants or animals performed by any of the authors.

Supplementary material

253_2017_8112_MOESM1_ESM.pdf (639 kb)
ESM 1 (PDF 639 kb)
253_2017_8112_MOESM2_ESM.xlsx (50 kb)
ESM 2 (XLSX 49 kb)

References

  1. Aguileta G, de Vienne DM, Ross ON, Hood ME, Giraud T, Petit E, Gabaldon T (2014) High variability of mitochondrial gene order among fungi. Genome Biol Evol 6(2):451–465CrossRefPubMedPubMedCentralGoogle Scholar
  2. Bensasson D (2001) Mitochondrial pseudogenes: evolution’s misplaced witnesses. Trends Ecol Evol 16(6):314–321CrossRefPubMedGoogle Scholar
  3. Benson G (1999) Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 27(2):573–580CrossRefPubMedPubMedCentralGoogle Scholar
  4. Brenner S, Johnson M, Bridgham J, Golda G, Lloyd DH, Johnson D, Luo S, McCurdy S, Foy M, Ewan M, Roth R, George D, Eletr S, Albrecht G, Vermaas E, Williams SR, Moon K, Burcham T, Pallas M, DuBridge RB, Kirchner J, Fearon K, Mao J-i, Corcoran K (2000) Gene expression analysis by massively parallel signature sequencing (MPSS) on microbead arrays. Nat Biotech 18(6):630–634CrossRefGoogle Scholar
  5. Chen L, Zhang QY, Jia M, Ming QL, Yue W, Rahman K, Qin LP, Han T (2016) Endophytic fungi with antitumor activities: their occurrence and anticancer compounds. Crit Rev Microbiol 42(3):454–473PubMedGoogle Scholar
  6. Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, Heger A, Hetherington K, Holm L, Mistry J, Sonnhammer EL, Tate J, Punta M (2014) Pfam: the protein families database. Nucleic Acids Res 42(Database issue):D222–D230CrossRefPubMedGoogle Scholar
  7. Hazkani-Covo E, Zeller RM, Martin W (2010) Molecular poltergeists: mitochondrial DNA copies (numts) in sequenced nuclear genomes. PLoS Genet 6(2):e1000834CrossRefPubMedPubMedCentralGoogle Scholar
  8. Huang Y, Niu B, Gao Y, Fu L, Li W (2010) CD-HIT Suite: a web server for clustering and comparing biological sequences. Bioinformatics 26:680–682CrossRefPubMedPubMedCentralGoogle Scholar
  9. Jaklitsch WM, Gardiennet A, Voglmayr H (2016) Resolution of morphology-based taxonomic delusions: Acrocordiella, Basiseptospora, Blogiascospora, Clypeosphaeria, Hymenopleella, Lepteutypa, Pseudapiospora, Requienella, Seiridium and Strickeria. Persoonia 37:82–105CrossRefPubMedPubMedCentralGoogle Scholar
  10. Jeewon R, Liew ECY, Hyde KD (2002) Phylogenetic relationships of Pestalotiopsis and allied genera inferred from ribosomal DNA sequences and morphological characters. Mol Phylogenet Evol 25(3):378–392CrossRefPubMedGoogle Scholar
  11. Kang X, Liu C, Liu D, Zeng L, Shi Q, Qian K, Xie B (2016) The complete mitochondrial genome of huperzine A-producing endophytic fungus Penicillium polonicum. Mitochondr DNA Part B 1(1):202–203CrossRefGoogle Scholar
  12. Kim D, Langmead B, Salzberg SL (2015) HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12(4):357–360CrossRefPubMedPubMedCentralGoogle Scholar
  13. Kurtz S, Schleiermacher C (1999) REPuter: fast computation of maximal repeats in complete genomes. Bioinformatics 15(5):426–427CrossRefPubMedGoogle Scholar
  14. Lanfear R, Calcott B, Ho SY, Guindon S (2012) Partitionfinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol Biol Evol 29(6):1695–1701CrossRefPubMedGoogle Scholar
  15. Laslett D, Canbäck B (2004) ARAGORN, a program to detect tRNA genes and tmRNA genes in nucleotide sequences. Nucleic Acids Res 32(1):11–16CrossRefPubMedPubMedCentralGoogle Scholar
  16. Laslett D, Canbäck B (2008) ARWEN: a program to detect tRNA genes in metazoan mitochondrial nucleotide sequences. Bioinformatics 24(2):172–175CrossRefPubMedGoogle Scholar
  17. Liu L (2011) Bioactive metabolites from the plant endophyte Pestalotiopsis fici. Mycology 2(1):37–45CrossRefGoogle Scholar
  18. Liu L, Liu S, Jiang L, Chen X, Guo L, Che Y (2008a) Chloropupukeananin, the first chlorinated pupukeanane derivative, and its precursors from Pestalotiopsis fici. Org Lett 10(7):1397–1400CrossRefPubMedGoogle Scholar
  19. Liu L, Tian RR, Liu SC, Chen XL, Guo LD, Che YS (2008b) Pestaloficiols A-E, bioactive cyclopropane derivatives from the plant endophytic fungus Pestalotiopsis fici. Bioorg Med Chem 16(11):6021–6026CrossRefPubMedGoogle Scholar
  20. Liu A-R, Chen S-C, Wu S-Y, Xu T, Guo L-D, Jeewon R, Wei J-G (2010) Cultural studies coupled with DNA based sequence analyses and its implication on pigmentation as a phylogenetic marker in Pestalotiopsis taxonomy. Mol Phylogenet Evol 57(2):528–535CrossRefPubMedGoogle Scholar
  21. Liu L, Bruhn T, Guo LD, Gotz DCG, Brun R, Stich A, Che YS, Bringmann G (2011) Chloropupukeanolides C-E: cytotoxic pupukeanane chlorides with a spiroketal skeleton from Pestalotiopsis fici. Chemi-Eur J 17(9):2604–2613CrossRefGoogle Scholar
  22. Liu L, Li Y, Li L, Cao Y, Guo L, Liu G, Che Y (2013) Spiroketals of Pestalotiopsis fici provide evidence for a biosynthetic hypothesis involving diversified Diels-Alder reaction cascades. J Org Chem 78(7):2992–3000CrossRefPubMedGoogle Scholar
  23. Liu L, Zhao C, Li L, Guo LD, Che YS (2015) Pestalotriols A and B, new spiro[2.5]octane derivatives from the endophytic fungus Pestalotiopsis fici. RSC Adv 5(96):78708–78711CrossRefGoogle Scholar
  24. Lowe TM, Eddy SR (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25(5):955–964CrossRefPubMedPubMedCentralGoogle Scholar
  25. Maharachchikumbura SSN, Guo LD, Chukeatirote E, Bahkali AH, Hyde KD (2011) Pestalotiopsis-morphology, phylogeny, biochemistry and diversity. Fungal Divers 50(1):167–187CrossRefGoogle Scholar
  26. Maharachchikumbura SSN, Hyde KD, Groenewald JZ, Xu J, Crous PW (2014) Pestalotiopsis revisited. Stud Mycol 79:121–186CrossRefPubMedPubMedCentralGoogle Scholar
  27. Martins M, Dairou J, Rodrigues-Lima F, Dupret JM, Silar P (2010) Insights into the phylogeny or arylamine N-acetyltransferases in fungi. J Mol Evol 71(2):141–152CrossRefPubMedGoogle Scholar
  28. Nadimi M, Daubois L, Hijri M (2016) Mitochondrial comparative genomics and phylogenetic signal assessment of mtDNA among arbuscular mycorrhizal fungi. Mol Phylogenet Evol 98:74–83CrossRefPubMedGoogle Scholar
  29. Rodriguez RJ, White JF Jr, Arnold AE, Redman RS (2009) Fungal endophytes: diversity and functional roles. New Phytol 182(2):314–330CrossRefPubMedGoogle Scholar
  30. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Hohna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61(3):539–542CrossRefPubMedPubMedCentralGoogle Scholar
  31. Senanayake IC, Maharachchikumbura SSN, Hyde KD, Bhat JD, Jones EBG, McKenzie EHC, Dai DQ, Daranagama DA, Dayarathne MC, Goonasekara ID, Konta S, Li WJ, Shang QJ, Stadler M, Wijayawardene NN, Xiao YP, Norphanphoun C, Li QR, Liu XZ, Bahkali AH, Kang JC, Wang Y, Wen TC, Wendt L, Xu JC, Camporesi E (2015) Towards unraveling relationships in Xylariomycetidae (Sordariomycetes). Fungal Divers 73(1):73–144CrossRefGoogle Scholar
  32. Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30(9):1312–1313CrossRefPubMedPubMedCentralGoogle Scholar
  33. Venugopalan A, Srivastava S (2015) Endophytes as in vitro production platforms of high value plant secondary metabolites. Biotechnol Adv 33(6, Part 1):873–887CrossRefPubMedGoogle Scholar
  34. Wagemaker MJ, Eastwood DC, Welagen J, van der Drift C, Jetten MS, Burton K, Van Griensven LJ, Op den Camp HJ (2007) The role of ornithine aminotransferase in fruiting body formation of the mushroom Agaricus bisporus. Mycol Res 111(Pt 8):909–918CrossRefPubMedGoogle Scholar
  35. Wang KW, Lei JX, Wei JG, Yao N (2012) Bioactive natural compounds from the plant endophytic fungi Pestalotiopsis spp. Mini-Rev Med Chem 12(13):1382–1393PubMedGoogle Scholar
  36. Wang X, Zhang X, Liu L, Xiang M, Wang W, Sun X, Che Y, Guo L, Liu G, Guo L, Wang C, Yin WB, Stadler M, Zhang X, Liu X (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(1):28CrossRefPubMedPubMedCentralGoogle Scholar
  37. Wang B, Zhang ZW, Guo LD, Liu L (2016) New cytotoxic meroterpenoids from the plant endophytic fungus Pestalotiopsis fici. Hel Chim Acta 99(2):151–156CrossRefGoogle Scholar
  38. Wu GW, Zhou HC, Zhang P, Wang XN, Li W, Zhang WW, Liu XZ, Liu HW, Keller NP, An ZQ, Yin WB (2016) Polyketide production of pestaloficiols and macrodiolide ficiolides revealed by manipulations of epigenetic regulators in an endophytic fungus. Org Lett 18(8):1832–1835CrossRefPubMedGoogle Scholar
  39. Zhang YJ, Zhang S, Liu XZ, Wen HA, Wang M (2010) A simple method of genomic DNA extraction suitable for analysis of bulk fungal strains. Lett Appl Microbiol 51(1):114–118PubMedGoogle Scholar
  40. Zhang Y, Zhang S, Zhang G, Liu X, Wang C, Xu J (2015) Comparison of mitochondrial genomes provides insights into intron dynamics and evolution in the caterpillar fungus Cordyceps militaris. Fungal Genet Biol 77:95–107CrossRefPubMedGoogle Scholar
  41. Zhang YJ, Zhao YX, Zhang S, Chen L, Liu XZ (2017) Reanalysis of the mitochondrial genome of the pneumocandin-producing fungus Glarea lozoyensis. Acta Microbiol Sin 2017 (in press)Google Scholar
  42. Zhu YY, Ai C, Zhang J, Zhang ZW, Zhao CQ (2011) Bioactive secondary metabolites from endophytic fungi in plants. Prog Chem 23(4):704–730Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Shu Zhang
    • 1
  • Xiu-Na Wang
    • 2
  • Xiao-Ling Zhang
    • 3
  • Xing-Zhong Liu
    • 3
  • Yong-Jie Zhang
    • 4
    Email author
  1. 1.Institute of Applied ChemistryShanxi UniversityTaiyuanChina
  2. 2.Fujian Agriculture and Forestry UniversityFuzhouChina
  3. 3.State Key Laboratory of Mycology, Institute of MicrobiologyChinese Academy of SciencesBeijingChina
  4. 4.School of Life SciencesShanxi UniversityTaiyuanChina

Personalised recommendations