Analysis of the complete mitochondrial genome of Pochonia chlamydosporia suggests a close relationship to the invertebrate-pathogenic fungi in Hypocreales

BMC Microbiology

Bingyan Xie³  Xinyue Cheng²  Zhenchuan Mao³  Guohua Chen³  Jian Ling³  Miao Bai¹  Baoming Shen⁴  Chichuan Liu³  Runmao Lin³ 

[1] Key Laboratory for Crop Germplasm Innovation and Utilization of Hunan Province, Hunan Agricultural University, Changsha 410128, Hunan Province, China;College of Life Sciences, Beijing Normal University, Beijing 100875, China;Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing 100081, China;College of Plant Protection, Hunan Agricultural University, Changsha 410128, Hunan Province, China

关键词: Phylogeny;    Evolution;    Rearrangement;    rps3;    Mitochondrial genome;    Biological control agent;    Pochonia chlamydosporia;    Nematode egg-parasite fungus;   

Others  :  1137663
DOI  :  10.1186/s12866-015-0341-8

 received in 2014-07-04, accepted in 2015-01-08,  发布年份 2015

【 摘 要 】

Background

The fungus Pochonia chlamydosporia parasitizes nematode eggs and has become one of the most promising biological control agents (BCAs) for plant-parasitic nematodes, which are major agricultural pests that cause tremendous economic losses worldwide. The complete mitochondrial (mt) genome is expected to open new avenues for understanding the phylogenetic relationships and evolution of the invertebrate-pathogenic fungi in Hypocreales.

Results

The complete mitogenome sequence of P. chlamydosporia is 25,615 bp in size, containing the 14 typical protein-coding genes, two ribosomal RNA genes, an intronic ORF coding for a putative ribosomal protein (rps3) and a set of 23 transfer RNA genes (trn) which recognize codons for all amino acids. Sequence similarity studies and syntenic gene analyses show that 87.02% and 58.72% of P. chlamydosporia mitogenome sequences match 90.50% of Metarhizium anisopliae sequences and 61.33% of Lecanicillium muscarium sequences with 92.38% and 86.04% identities, respectively. A phylogenetic tree inferred from 14 mt proteins in Pezizomycotina fungi supports that P. chlamydosporia is most closely related to the entomopathogenic fungus M. anisopliae. The invertebrate-pathogenic fungi in Hypocreales cluster together and clearly separate from a cluster comprising plant-pathogenic fungi (Fusarium spp.) and Hypocrea jecorina. A comparison of mitogenome sizes shows that the length of the intergenic regions or the intronic regions is the major size contributor in most of mitogenomes in Sordariomycetes. Evolutionary analysis shows that rps3 is under positive selection, leading to the display of unique evolutionary characteristics in Hypocreales. Moreover, the variability of trn distribution has a clear impact on gene order in mitogenomes. Gene rearrangement analysis shows that operation of transposition drives the rearrangement events in Pezizomycotina, and most events involve in trn position changes, but no rearrangement was found in Clavicipitaceae.

Conclusions

We present the complete annotated mitogenome sequence of P. chlamydosporia. Based on evolutionary and phylogenetic analyses, we have determined the relationships between the invertebrate-pathogenic fungi in Hypocreales. The invertebrate-pathogenic fungi in Hypocreales referred to in this paper form a monophyletic group sharing a most recent common ancestor. Our rps3 and trn gene order results also establish a foundation for further exploration of the evolutionary trajectory of the fungi in Hypocreales.

【 授权许可】

   
2015 Lin et al.; licensee BioMed Central.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

【 参考文献 】

• [1]Escudero N, Lopez-Llorca LV: Effects on plant growth and root-knot nematode infection of an endophytic GFP transformant of the nematophagous fungus Pochonia chlamydosporia. Symbiosis 2012, 57(1):33-42.
• [2]Manzanilla-López RH, Esteves I, Finetti-Sialer MM, Hirsch PR, Ward E, Devonshire J, et al.: Pochonia chlamydosporia: advances and challenges to improve its performance as a biological control agent of sedentary endo-parasitic nematodes. Journal of Nematology 2013, 45(1):1.
• [3]Kerry BR: Rhizosphere interactions and the exploitation of microbial agents for the biological control of plant-parasitic nematodes. Annu Rev Phytopathol 2000, 38:423-41.
• [4]Kerry BR, Bourne JM: The importance of rhizosphere interactions in the biological control of plant parasitic nematodes—a case study using Verticillium chlamydosporium. Pesticide Science 1996, 47(1):69-75.
• [5]Casas-Flores S, Herrera-Estrella A: Antagonism of plant parasitic nematodes by fungi. In The mycota IV: environmental and microbial relationships. 2nd edition. Edited by Kubicek C, Druzhinina I. Springer, Berlin, Germany; 2007:147-57.
• [6]Sasser J, Freckman D: A world perspective on nematology: the role of the society. In Vistas on nematology. Edited by Veech JA, Dickson DW. Society of Nematologists, Hyatsville, MD USA; 1987:7-14.
• [7]Zare R, Gams W, Evans H: A revision of Verticillium section Prostrata. V. The genus Pochonia, with notes on Rotiferophthora. Nova Hedwigia 2001, 73(1):51-86.
• [8]Morton CO, Mauchline TH, Kerry R, Hirsch PR: PCR-based DNA fingerprinting indicates host-related genetic variation in the nematophagous fungus Pochonia chlamydosporia. Mycol Res 2003, 107(2):198-205.
• [9]Nikoh N, Fukatsu T: Interkingdom host jumping underground: phylogenetic analysis of entomoparasitic fungi of the genus cordyceps. Mol Biol Evol 2000, 17(4):629-38.
• [10]Sung G-H, Sung J-M, Hywel-Jones NL, Spatafora JW: A multi-gene phylogeny of Clavicipitaceae (Ascomycota, Fungi): Identification of localized incongruence using a combinational bootstrap approach. Mol Phylogenet Evol 2007, 44(3):1204-23.
• [11]Larriba E, Jaime MD, Carbonell-Caballero J, Conesa A, Dopazo J, Nislow C, et al.: Sequencing and functional analysis of the genome of a nematode egg-parasitic fungus, Pochonia chlamydosporia. Fungal Genet Biol 2014, 65:69-80.
• [12]Duò A, Bruggmann R, Zoller S, Bernt M, Grünig CR: Mitochondrial genome evolution in species belonging to the Phialocephala fortinii s.l. - Acephala applanata species complex. BMC Genomics 2012, 13(1):166. BioMed Central Full Text
• [13]Paquin B, Laforest M-J, Forget L, Roewer I, Wang Z, Longcore J, et al.: The fungal mitochondrial genome project: evolution of fungal mitochondrial genomes and their gene expression. Curr Genet 1997, 31(5):380-95.
• [14]Gray MW. Mitochondrial evolution. Cold Spring Harbor Perspectives in Biology. 2012; 4(9):a011403
• [15]Zheng A, Lin R, Zhang D, Qin P, Xu L, Ai P, et al.: The evolution and pathogenic mechanisms of the rice sheath blight pathogen. Nat Commun 2013, 4:1424.
• [16]Pramateftaki PV, Kouvelis VN, Lanaridis P, Typas MA: The mitochondrial genome of the wine yeast Hanseniaspora uvarum: a unique genome organization among yeast/fungal counterparts. FEMS Yeast Res 2006, 6(1):77-90.
• [17]Belcour L, Rossignol M, Koll F, Sellem CH, Oldani C: Plasticity of the mitochondrial genome in Podospora. Polymorphism for 15 optional sequences: group-I, group-II introns, intronic ORFs and an intergenic region. Curr Genet 1997, 31(4):308-17.
• [18]Hausner G: Fungal mitochondrial genomes, plasmids and introns. Applied Mycology and Biotechnology 2003, 3:101-31.
• [19]Formighieri EF, Tiburcio RA, Armas ED, Medrano FJ, Shimo H, Carels N, et al.: The mitochondrial genome of the phytopathogenic basidiomycete Moniliophthora perniciosa is 109 kb in size and contains a stable integrated plasmid. Mycol Res 2008, 112(10):1136-52.
• [20]Sethuraman J, Majer A, Friedrich N, Edgell D, Hausner G: Genes within genes: multiple LAGLIDADG homing endonucleases target the ribosomal protein S3 gene encoded within an rnl group I intron of Ophiostoma and related taxa. Mol Biol Evol 2009, 26(10):2299-315.
• [21]Sethuraman J, Majer A, Iranpour M, Hausner G: Molecular evolution of the mtDNA encoded rps3 gene among filamentous ascomycetes fungi with an emphasis on the ophiostomatoid fungi. J Mol Evol 2009, 69(4):372-85.
• [22]Aguileta G, de Vienne DM, Ross ON, Hood ME, Giraud T, Petit E, et al.: High variability of mitochondrial gene order among fungi. Genome Biol Evol 2014, 6(2):451-65.
• [23]Tuller T, Girshovich Y, Sella Y, Kreimer A, Freilich S, Kupiec M, et al.: Association between translation efficiency and horizontal gene transfer within microbial communities. Nucleic Acids Res 2011, 39(11):4743-55.
• [24]Ghikas DV, Kouvelis VN, Typas MA: The complete mitochondrial genome of the entomopathogenic fungus Metarhizium anisopliae var. anisopliae: gene order and trn gene clusters reveal a common evolutionary course for all Sordariomycetes, while intergenic regions show variation. Arch Microbiol 2006, 185(5):393-401.
• [25]Pantou MP, Kouvelis VN, Typas MA: The complete mitochondrial genome of Fusarium oxysporum: Insights into fungal mitochondrial evolution. Gene 2008, 419(1):7-15.
• [26]Xu J, Huang B, Qin C, Li Z-Z: Sequence and phylogenetic analysis of Beauveria bassiana with mitochondrial genome. Mycosystema 2009, 28(5):718-23.
• [27]Perseke M, Fritzsch G, Ramsch K, Bernt M, Merkle D, Middendorf M, et al.: Evolution of mitochondrial gene orders in echinoderms. Mol Phylogenet Evol 2008, 47(2):855-64.
• [28]Cameron SL, Yoshizawa K, Mizukoshi A, Whiting MF, Johnson KP: Mitochondrial genome deletions and minicircles are common in lice (Insecta: Phthiraptera). BMC Genomics 2011, 12:394. BioMed Central Full Text
• [29]Saccone C, Gissi C, Reyes A, Larizza A, Sbisa E, Pesole G: Mitochondrial DNA in metazoa: degree of freedom in a frozen event. Gene 2002, 286(1):3-12.
• [30]Kouvelis VN, Ghikas DV, Typas MA: The analysis of the complete mitochondrial genome of Lecanicillium muscarium (synonym Verticillium lecanii) suggests a minimum common gene organization in mtDNAs of Sordariomycetes: phylogenetic implications. Fungal Genet Biol 2004, 41(10):930-40.
• [31]Lohse M, Drechsel O, Kahlau S, Bock R. OrganellarGenomeDRAW--a suite of tools for generating physical maps of plastid and mitochondrial genomes and visualizing expression data sets. Nucleic Acids Res. 2013;41(Web Server issue):W575–81.
• [32]Pantou MP, Kouvelis VN, Typas MA: The complete mitochondrial genome of the vascular wilt fungus Verticillium dahliae: a novel gene order for Verticillium and a diagnostic tool for species identification. Curr Genet 2006, 50(2):125-36.
• [33]Fox TD: Natural variation in the genetic code. Annu Rev Genet 1987, 21(1):67-91.
• [34]Yang Z: PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 2007, 24(8):1586-91.
• [35]Yang Z, Nielsen R: Codon-substitution models for detecting molecular adaptation at individual sites along specific lineages. Mol Biol Evol 2002, 19(6):908-17.
• [36]Anisimova M, Bielawski JP, Yang Z: Accuracy and power of the likelihood ratio test in detecting adaptive molecular evolution. Mol Biol Evol 2001, 18(8):1585-92.
• [37]Librado P, Rozas J: DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 2009, 25(11):1451-2.
• [38]Sung G-H. Complete mitochondrial DNA genome of the medicinal mushroom Cordyceps militaris (Ascomycota, Cordycipitaceae). Mitochondrial DNA. 2013 http://dx.doi.org/10.3109/19401736.2013.855754 (in press).
• [39]Juhász Á, Pfeiffer I, Keszthelyi A, Kucsera J, Vágvölgyi C, Hamari Z: Comparative analysis of the complete mitochondrial genomes of Aspergillus niger mtDNA type 1a and Aspergillus tubingensis mtDNA type 2b. FEMS Microbiol Lett 2008, 281(1):51-7.
• [40]Bernt M, Merkle D, Ramsch K, Fritzsch G, Perseke M, Bernhard D, et al.: CREx: inferring genomic rearrangements based on common intervals. Bioinformatics 2007, 23(21):2957-8.
• [41]Morton CO, Hirsch PR, Peberdy JP, Kerry BR: Cloning of and genetic variation in protease VCP1 from the nematophagous fungus Pochonia chlamydosporia. Mycol Res 2003, 107(1):38-46.
• [42]Larriba E, Martín-Nieto J, Lopez-Llorca LV: Gene cloning, molecular modeling, and phylogenetics of serine protease P32 and serine carboxypeptidase SCP1 from nematophagous fungi Pochonia rubescens and Pochonia chlamydosporia. Can J Microbiol 2012, 58(7):815-27.
• [43]Shimazu M, Mitsuhashi W, Hashimoto H: Cordyceps brongniartii sp. nov., the teleomorph of Beauveria brongniartii. Transactions of the Mycological Society of Japan 1988, 29:323-30.
• [44]Zare R, Gams W: A revision of Verticillium section Prostrata. IV. The genera Lecanicillium and Simplicillium gen. nov. Nova Hedwigia 2001, 73(1–2):1-50.
• [45]Li Z, Li C, Huang B, Fan M: Discovery and demonstration of the teleomorph of Beauveria bassiana (Bals.) Vuill., an important entomogenous fungus. Chinese Science Bulletin 2001, 46(9):751-3.
• [46]Kuhls K, Lieckfeldt E, Samuels GJ, Kovacs W, Meyer W, Petrini O, et al.: Molecular evidence that the asexual industrial fungus Trichoderma reesei is a clonal derivative of the ascomycete Hypocrea jecorina. Proc Natl Acad Sci U S A 1996, 93(15):7755-60.
• [47]Lee J, Young JPW: The mitochondrial genome sequence of the arbuscular mycorrhizal fungus Glomus intraradices isolate 494 and implications for the phylogenetic placement of Glomus. New Phytologist 2009, 183(1):200-11.
• [48]Xiao G, Ying SH, Zheng P, Wang ZL, Zhang S, Xie XQ, et al.: Genomic perspectives on the evolution of fungal entomopathogenicity in Beauveria bassiana. Sci Rep 2012, 2:483.
• [49]Ran JH, Gao H, Wang XQ: Fast evolution of the retroprocessed mitochondrial rps3 gene in Conifer II and further evidence for the phylogeny of gymnosperms. Mol Phylogenet Evol 2010, 54(1):136-49.
• [50]Kim Y, Kim HD, Kim J: Cytoplasmic ribosomal protein S3 (rpS3) plays a pivotal role in mitochondrial DNA damage surveillance. Biochim Biophys Acta 2013, 1833(12):2943-52.
• [51]Fountaine J, Shaw M, Napier B, Ward E, Fraaije B: Application of real-time and multiplex polymerase chain reaction assays to study leaf blotch epidemics in barley. Phytopathology 2007, 97(3):297-303.
• [52]Gnerre S, MacCallum I, Przybylski D, Ribeiro FJ, Burton JN, Walker BJ, et al.: High-quality draft assemblies of mammalian genomes from massively parallel sequence data. Proc Natl Acad Sci U S A 2011, 108(4):1513-8.
• [53]Li H, Durbin R: Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 2009, 25(14):1754-60.
• [54]Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al.: The sequence alignment/map format and SAMtools. Bioinformatics 2009, 25(16):2078-9.
• [55]Consortium U: Update on activities at the universal protein resource (UniProt) in 2013. Nucleic Acids Res 2013, 41(D1):D43-7.
• [56]Slater GS, Birney E: Automated generation of heuristics for biological sequence comparison. BMC Bioinformatics 2005, 6(1):31. BioMed Central Full Text
• [57]Lowe TM, Eddy SR: tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 1997, 25(5):0955-64.
• [58]Burge SW, Daub J, Eberhardt R, Tate J, Barquist L, Nawrocki EP, et al.: Rfam 11.0: 10 years of RNA families. Nucleic Acids Res 2013, 41(D1):D226-32.
• [59]RepeatMasker. [http://www.repeatmasker.org/]
• [60]EMBOSS einverted and palindrome. [http://emboss.bioinformatics.nl/cgi-bin/emboss/]
• [61]Ghikas DV, Kouvelis VN, Typas MA: Phylogenetic and biogeographic implications inferred by mitochondrial intergenic region analyses and ITS1-5.8 S-ITS2 of the entomopathogenic fungi Beauveria bassiana and B. brongniartii. BMC Microbiol 2010, 10(1):174. BioMed Central Full Text
• [62]Pantou MP, Strunnikova OK, Shakhnazarova VY, Vishnevskaya NA, Papalouka VG, Typas MA: Molecular and immunochemical phylogeny of Verticillium species. Mycol Res 2005, 109(8):889-902.
• [63]Neurospora crassa database. [http://www.broadinstitute.org/annotation/genome/neurospora/MultiHome.html]
• [64]Chambergo FS, Bonaccorsi ED, Ferreira AJ, Ramos AS, Ferreira JR, Abrahao-Neto J, et al.: Elucidation of the metabolic fate of glucose in the filamentous fungus Trichoderma reesei using expressed sequence tag (EST) analysis and cDNA microarrays. Journal of Biological Chemistry 2002, 277(16):13983-8.
• [65]Al-Reedy RM, Malireddy R, Dillman CB, Kennell JC: Comparative analysis of Fusarium mitochondrial genomes reveals a highly variable region that encodes an exceptionally large open reading frame. Fungal Genet Biol 2012, 49(1):2-14.
• [66]Joardar V, Abrams NF, Hostetler J, Paukstelis PJ, Pakala S, Pakala SB, et al.: Sequencing of mitochondrial genomes of nine Aspergillus and Penicillium species identifies mobile introns and accessory genes as main sources of genome size variability. BMC Genomics 2012, 13(1):698. BioMed Central Full Text
• [67]Juhász Á, Engi H, Pfeiffer I, Kucsera J, Vágvölgyi C, Hamari Z: Interpretation of mtDNA RFLP variability among Aspergillus tubingensis isolates. Antonie Van Leeuwenhoek 2007, 91(3):209-16.
• [68]Wu Y, Yang J, Yang F, Liu T, Leng W, Chu Y, et al.: Recent dermatophyte divergence revealed by comparative and phylogenetic analysis of mitochondrial genomes. BMC Genomics 2009, 10(1):238. BioMed Central Full Text
• [69]Tambor JHM, Guedes RF, Nobrega MP, Nobrega FG: The complete DNA sequence of the mitochondrial genome of the dermatophyte fungus Epidermophyton floccosum. Curr Genet 2006, 49(5):302-8.
• [70]Cardoso MAG, Tambor JHM, Nobrega FG: The mitochondrial genome from the thermal dimorphic fungus Paracoccidioides brasiliensis. Yeast 2007, 24(7):607-16.
• [71]CREx web server. [http://pacosy.informatik.uni-leipzig.de/crex]
• [72]Edgar RC: MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004, 32(5):1792-7.
• [73]Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, Chevenet F, et al.: Phylogeny. fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 2008, 36(2):W465-9.
• [74]Darriba D, Taboada GL, Doallo R, Posada D: jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 2012, 9(8):772.
• [75]Akaike H. Information theory and an extension of the maximum likelihood principle. In: Second international symposium on information theory. Akademinai Kiado: 1973; 267–281.
• [76]Schwarz G: Estimating the dimension of a model. The Annals of Statistics 1978, 6(2):461-4.
• [77]Tavaré S: Some probabilistic and statistical problems in the analysis of DNA sequences. Lectures on Mathematics in the Life Sciences 1986, 17:57-86.
• [78]Tamura K, Stecher G, Peterson D, Filipski A, Kumar S: MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 2013, 30(12):2725-9.
• [79]Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel O: New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 2010, 59(3):307-21.
• [80]Darriba D, Taboada GL, Doallo R, Posada D: ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 2011, 27(8):1164-5.
• [81]Adachi J, Waddell PJ, Martin W, Hasegawa M: Plastid genome phylogeny and a model of amino acid substitution for proteins encoded by chloroplast DNA. J Mol Evol 2000, 50(4):348-58.
• [82]Jones DT, Taylor WR, Thornton JM: The rapid generation of mutation data matrices from protein sequences. Computer Applications in the Biosciences: CABIOS 1992, 8(3):275-82.
• [83]Phylogenetic data. [http://purl.org/phylo/treebase/phylows/study/TB2:S16935]