Abstract
In the present study, we assembled the mitogenomes of Pleurotus citrinopileatus and Pleurotus platypus. The circular mitogenome of the two Pleurotus species comprises a set of 14 conserved protein-encoding genes (PEGs), 2 RNA genes (small subunit ribosomal RNA and large subunit ribosomal RNA), and 24 tRNAs, with sizes of 60,694 and 73,807 bp, respectively. They contain 4 and 10 introns with 3 and 10 intronic open reading frames (ORFs), respectively. Thirteen position classes (Pcls) of introns were found in the cox1 gene of four Pleurotus species. The number and class of Pcl varied among different Pleurotus species, indicating that numerous events of loss and gain occurred during evolution of Pleurotus. Comparative mitogenomic and collinearity analyses reveal that large-scale gene rearrangements may have occurred during the evolution of Pleurotus citrinopileatus and Pleurotus platypus, including gene rearrangements and inversions, which may be related to the observed high amounts of repetitive DNA elements (5.62 and 5.45%, respectively). Phylogenetic analysis based on concatenated mitochondrial protein sequences reveals that concatenated mitochondrial genes are suitable as molecular markers for phylogenetic analysis. This serves as the first report on large-scale rearrangements in the mitochondria of the genus Pleurotus, thereby improving our understanding of the evolution of the Pleurotus genus and other macrofungi.
Similar content being viewed by others
References
Ademola IO, Odeniran PO (2017) Novel trypanocide from an extract of Pleurotus sajor-caju against Trypanosoma congolense. Pharm Biol 55(1):132–138. https://doi.org/10.1080/13880209.2016.1230878
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):451–465. https://doi.org/10.1093/gbe/evu028
Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19(5):455–477. https://doi.org/10.1089/cmb.2012.0021
Belfort M, Bonocora RP (2014) Homing endonucleases: from genetic anomalies to programmable genomic clippers. Methods Mol Biol 1123:1–26. https://doi.org/10.1007/978-1-62703-968-0_1
Benson G (1999) Tandem repeats finder: a program to analyze DNA sequences. Nat Rev Nephrol 27(2):573–580
Boore JL (1999) Animal mitochondrial genomes. Nucleic Acids Res 27(8):1767–1780. https://doi.org/10.1093/nar/27.8.1767
Brabec J, Kostadinova A, Scholz T, Littlewood DT (2015) Complete mitochondrial genomes and nuclear ribosomal RNA operons of two species of Diplostomum (Platyhelminthes: Trematoda): a molecular resource for taxonomy and molecular epidemiology of important fish pathogens. Parasit Vectors 8:336. https://doi.org/10.1186/s13071-015-0949-4
Brankovics B, van Dam P, Rep M, de Hoog GS, TA JvdL, Waalwijk C, van Diepeningen AD (2017) Mitochondrial genomes reveal recombination in the presumed asexual Fusarium oxysporum species complex. BMC Genomics 18(1):735 doi:https://doi.org/10.1186/s12864-017-4116-5
Castro-Alves VC, Gomes D, Menolli N, Jr., Sforca ML, Nascimento JR (2017) Characterization and immunomodulatory effects of glucans from Pleurotus albidus, a promising species of mushroom for farming and biomass production. Int J Biol Macromol 95:215–223 doi:https://doi.org/10.1016/j.ijbiomac.2016.11.059
Chen L, Zhang Y, Sha O, Xu W, Wang S (2016) Hypolipidaemic and hypoglycaemic activities of polysaccharide from Pleurotus eryngii in Kunming mice. Int J Biol Macromol 93(Pt A) 93:1206–1209. https://doi.org/10.1016/j.ijbiomac.2016.09.094
Choi JH, Kim DW, Kim S, Kim SJ (2017) In vitro antioxidant and in vivo hypolipidemic effects of the king oyster qulinary-medicinal mushroom, Pleurotus eryngii var. ferulae DDL01 (Agaricomycetes), in rats with high-fat diet-induced fatty liver and hyperlipidemia. Int J Med Mushrooms 19(2):107–119. https://doi.org/10.1615/IntJMedMushrooms.v19.i2.20
Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9(8):772. https://doi.org/10.1038/nmeth.2109
Einer C, Hohenester S, Wimmer R, Wottke L, Artmann R, Schulz S, Gosmann C, Simmons A, Leitzinger C, Eberhagen C, Borchard S, Schmitt S, Hauck SM, von Toerne C, Jastroch M, Walheim E, Rust C, Gerbes AL, Popper B, Mayr D, Schnurr M, Vollmar AM, Denk G, Zischka H (2018) Mitochondrial adaptation in steatotic mice. Mitochondrion 40:1–12. https://doi.org/10.1016/j.mito.2017.08.015
Ferandon C, Moukha S, Callac P, Benedetto JP, Castroviejo M, Barroso G (2010) The Agaricus bisporus cox1 gene: the longest mitochondrial gene and the largest reservoir of mitochondrial group I introns. PLoS One 5(11):e14048. https://doi.org/10.1371/journal.pone.0014048
Ferandon C, Xu J, Barroso G (2013) The 135 kbp mitochondrial genome of Agaricus bisporus is the largest known eukaryotic reservoir of group I introns and plasmid-related sequences. Fungal Genet Biol 55:85–91. https://doi.org/10.1016/j.fgb.2013.01.009
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–D230. https://doi.org/10.1093/nar/gkt1223
Forget L, Ustinova J, Wang Z, Huss VA, Lang BF (2002) Hyaloraphidium curvatum: a linear mitochondrial genome, tRNA editing, and an evolutionary link to lower fungi. Mol Biol Evol 19(3):310–319
Formighieri EF, Tiburcio RA, Armas ED, Medrano FJ, Shimo H, Carels N, Goes-Neto A, Cotomacci C, Carazzolle MF, Sardinha-Pinto N, Thomazella DP, Rincones J, Digiampietri L, Carraro DM, Azeredo-Espin AM, Reis SF, Deckmann AC, Gramacho K, Goncalves MS, Moura Neto JP, Barbosa LV, Meinhardt LW, Cascardo JC, Pereira GA (2008) The mitochondrial genome of the phytopathogenic basidiomycete Moniliophthora perniciosa is 109 kb in size and contains a stable integrated plasmid. Mycol Res 112(Pt 10):1136–1152. https://doi.org/10.1016/j.mycres.2008.04.014
Fu Y, Dai Y, Yang C, Wei P, Song B, Yang Y, Sun L, Zhang ZW, Li Y (2017) Comparative transcriptome analysis identified candidate genes related to Bailinggu mushroom formation and genetic markers for genetic analyses and breeding. Sci Rep 7(1):9266. https://doi.org/10.1038/s41598-017-08049-z
Garcia-Betancur JC, Menendez MC, Del Portillo P, Garcia MJ (2012) Alignment of multiple complete genomes suggests that gene rearrangements may contribute towards the speciation of Mycobacteria. Infect Genet Evol 12(4):819–826. https://doi.org/10.1016/j.meegid.2011.09.024
Hahn C, Bachmann L, Chevreux B (2013) Reconstructing mitochondrial genomes directly from genomic next-generation sequencing reads—a baiting and iterative mapping approach. Nucleic Acids Res 41(13):e129. https://doi.org/10.1093/nar/gkt371
Hazkani-Covo E, Zeller RM, Martin W (2010) Molecular poltergeists: mitochondrial DNA copies (numts) in sequenced nuclear genomes. PLoS Genet 6(2):e1000834. https://doi.org/10.1371/journal.pgen.1000834
Himmelstrand K, Olson A, Brandstrom Durling M, Karlsson M, Stenlid J (2014) Intronic and plasmid-derived regions contribute to the large mitochondrial genome sizes of Agaricomycetes. Curr Genet 60(4):303–313. https://doi.org/10.1007/s00294-014-0436-z
Jimenez M, Goodchild SC, Stockwell CA, Lema SC (2017) Characterization and phylogenetic analysis of complete mitochondrial genomes for two desert cyprinodontoid fishes, Empetrichthys latos and Crenichthys baileyi. Gene 626:163–172. https://doi.org/10.1016/j.gene.2017.05.023
Kang X, Hu L, Shen P, Li R, Liu D (2017) SMRT sequencing revealed mitogenome characteristics and mitogenome-wide DNA modification pattern in Ophiocordyceps sinensis. Front Microbiol 8:1422. https://doi.org/10.3389/fmicb.2017.01422
Kanzi AM, Wingfield BD, Steenkamp ET, Naidoo S, van der Merwe NA (2016) Intron derived size polymorphism in the mitochondrial genomes of closely related Chrysoporthe species. PLoS One 11(6):e0156104. https://doi.org/10.1371/journal.pone.0156104
Kurtz S, Choudhuri JV, Ohlebusch E, Schleiermacher C, Stoye J, Giegerich R (2001) REPuter: the manifold applications of repeat analysis on a genomic scale. Nucleic Acids Res 29(22):4633–4642
Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9(4):357–359. https://doi.org/10.1038/nmeth.1923
Losada L, Pakala SB, Fedorova ND, Joardar V, Shabalina SA, Hostetler J, Pakala SM, Zafar N, Thomas E, Rodriguez-Carres M, Dean R, Vilgalys R, Nierman WC, Cubeta MA (2014) Mobile elements and mitochondrial genome expansion in the soil fungus and potato pathogen Rhizoctonia solani AG-3. FEMS Microbiol Lett 352(2):165–173. https://doi.org/10.1111/1574-6968.12387
Lowe TM, Chan PP (2016) tRNAscan-SE On-line: integrating search and context for analysis of transfer RNA genes. Nucleic Acids Res 44(W1):W54–W57. https://doi.org/10.1093/nar/gkw413
Pramateftaki PV, Kouvelis VN, Lanaridis P, Typas MA (2006) The mitochondrial genome of the wine yeast Hanseniaspora uvarum: a unique genome organization among yeast/fungal counterparts. FEMS Yeast Res 6(1):77–90. https://doi.org/10.1111/j.1567-1364.2005.00018.x
Riley R, Salamov AA, Brown DW, Nagy LG, Floudas D, Held BW, Levasseur A, Lombard V, Morin E, Otillar R, Lindquist EA, Sun H, LaButti KM, Schmutz J, Jabbour D, Luo H, Baker SE, Pisabarro AG, Walton JD, Blanchette RA, Henrissat B, Martin F, Cullen D, Hibbett DS, Grigoriev IV (2014) Extensive sampling of basidiomycete genomes demonstrates inadequacy of the white-rot/brown-rot paradigm for wood decay fungi. Proc Natl Acad Sci U S A 111(27):9923–9928 doi:https://doi.org/10.1073/pnas.1400592111
Ronquist F, Teslenko M, Van Der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61(3):539–542. https://doi.org/10.1093/sysbio/sys029
Shen XY, Li T, Chen S, Fan L, Gao J, Hou CL (2015) Characterization and phylogenetic analysis of the mitochondrial genome of Shiraia bambusicola reveals special features in the order of Pleosporales. PLoS One 10(3):e0116466. https://doi.org/10.1371/journal.pone.0116466
Shi W, Miao XG, Kong XY (2014) A novel model of double replications and random loss accounts for rearrangements in the mitogenome of Samariscus latus (Teleostei: Pleuronectiformes). BMC Genomics 15:352. https://doi.org/10.1186/1471-2164-15-352
Valach M, Burger G, Gray MW, Lang BF (2014) Widespread occurrence of organelle genome-encoded 5S rRNAs including permuted molecules. Nucleic Acids Res 42(22):13764–13777. https://doi.org/10.1093/nar/gku1266
Wang Y, Zeng F, Hon CC, Zhang Y, Leung FC (2008) The mitochondrial genome of the Basidiomycete fungus Pleurotus ostreatus (oyster mushroom). FEMS Microbiol Lett 280(1):34–41. https://doi.org/10.1111/j.1574-6968.2007.01048.x
Wang J, Zhang L, Zhang QL, Zhou MQ, Wang XT, Yang XZ, Yuan ML (2017) Comparative mitogenomic analysis of mirid bugs (Hemiptera: Miridae) and evaluation of potential DNA barcoding markers. PeerJ 5:e3661. https://doi.org/10.7717/peerj.3661
Yamasaki H, Izumiyama S, Nozaki T (2017) Complete sequence and characterization of the mitochondrial genome of Diphyllobothrium stemmacephalum, the type species of genus Diphyllobothrium (Cestoda: Diphyllobothriidae), using next generation sequencing. Parasitol Int 66(5):573–578. https://doi.org/10.1016/j.parint.2017.06.005
Yang R, Li Y, Song X, Tang L, Li C, Tan Q, Bao D (2017) The complete mitochondrial genome of the widely cultivated edible fungus Lentinula edodes. Mitochondrial DNA Part B 2(1):13–14. https://doi.org/10.1080/23802359.2016.1275839
Yao J, Yang H, Dai R (2017) Characterization of the complete mitochondrial genome of Acanthoscelides obtectus (Coleoptera: Chrysomelidae: Bruchinae) with phylogenetic analysis. Genetica 145(4–5):397–408. https://doi.org/10.1007/s10709-017-9975-9
Yoon H, You YH, Woo JR, Park YJ, Kong WS, Lee BM, Kim JG (2012) The mitochondrial genome of the white-rot fungus Flammulina velutipes. J Gen Appl Microbiol 58(4):331–337
Yuan X, Feng C, Zhang Z, Zhang C (2017) Complete mitochondrial genome of Phytophthora nicotianae and identification of molecular markers for the Oomycetes. Front Microbiol 8:1484. https://doi.org/10.3389/fmicb.2017.01484
Zhang YJ, Zhang S, Liu XZ (2016) The complete mitochondrial genome of the nematode endoparasitic fungus Hirsutella minnesotensis. Mitochondrial DNA A DNA Mapp Seq Anal 27(4):2693–2694. https://doi.org/10.3109/19401736.2015.1046126
Zhang B, Zhang YH, Wang X, Zhang HX, Lin Q (2017a) The mitochondrial genome of a sea anemone Bolocera sp. exhibits novel genetic structures potentially involved in adaptation to the deep-sea environment. Ecol Evol 7(13):4951–4962. https://doi.org/10.1002/ece3.3067
Zhang S, Wang XN, Zhang XL, Liu XZ, Zhang YJ (2017b) Complete mitochondrial genome of the endophytic fungus Pestalotiopsis fici: features and evolution. Appl Microbiol Biotechnol 101(4):1593–1604. https://doi.org/10.1007/s00253-017-8112-0
Zhang YJ, Zhang HY, Liu XZ, Zhang S (2017c) Mitochondrial genome of the nematode endoparasitic fungus Hirsutella vermicola reveals a high level of synteny in the family Ophiocordycipitaceae. Appl Microbiol Biotechnol 101(8):3295–3304. https://doi.org/10.1007/s00253-017-8257-x
Acknowledgments
We thank LetPub (www.letpub.com) for its linguistic assistance during the preparation of this manuscript. We thank Qiangfeng Wang for helping to do the requested final changes to the paper.
Funding
This study was funded by the National Science & Technology Pillar Program of Sichuan (2016NZ0042) and the Crop Molecular Breeding Platform in Sichuan (2016NZ0103).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
This article does not contain any studies with human participants performed by any of the authors.
Rights and permissions
About this article
Cite this article
Li, Q., Chen, C., Xiong, C. et al. Comparative mitogenomics reveals large-scale gene rearrangements in the mitochondrial genome of two Pleurotus species. Appl Microbiol Biotechnol 102, 6143–6153 (2018). https://doi.org/10.1007/s00253-018-9082-6
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-018-9082-6