Abstract
In the present study, the mitochondrial genomes of Peltigera elisabethae and P. polydactylon were sequenced and assembled. The two mitogenomes were composed of circular DNA molecules, with sizes of 64,034 bp and 59,208 bp, respectively. Comparative analysis showed that the genome size, GC content, GC skew, and AT skew varied between the two mitochondrial genomes. In codon analysis, phenylalanine (Phe), isoleucine (Ile), and leucine (Leu) were most frequently used in six Peltigera genomes. Evolutionary analysis showed that all 14 protein-coding genes (PCGs) were subject to purifying selection in the six Peltigera species. Regarding gene rearrangement, the PCGs of Peltigera had the same gene sequence and gene content, and a few intron sequences and spacer sequences were rearranged in Peltigera. In the phylogenetic analysis, we used Bayesian and ML methods to construct a phylogenetic tree. Two phylogenetic trees with consistent topology with high support indicate that mitochondrial genes were reliable molecular markers for analyzing the phylogenetic relationships. The present study enriches the mitochondrial genome data of Peltigera and promotes further understanding of the genetics and evolution of the Peltigera genus.
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References
Abbas A, Wu JN (1998) Lichens of Xinjiang. Science Technology & Hygiene Publishing House of Xinjiang, Urumqi, Xinjiang
Aguileta G, De Vienne DM, Ross ON, Hood ME, Giraud T, Petit E, Gabaldón T (2014) High variability of mitochondrial gene order among fungi. Genome Biol Evol 6(2):451–465. https://doi.org/10.1093/gbe/evu028
Aras S, Duman DC (2006) Isolation of DNA for sequence analysis from herbarium material of some lichen specimens. Turk J Bot 30(6):449–453
Barr CM, Neiman M, Taylor DR (2005) Inheritance and recombination of mitochondrial genomes in plants, fungi and animals. New Phytol 168(1):39–50. https://doi.org/10.1111/j.1469-8137.2005.01492.x
Bietenhader M, Martos A, Tetaud E, Aiyar RS, Sellem CH, Kucharczyk R, Di Rago JP (2012) Experimental relocation of the mitochondrial atp9 gene to the nucleus reveals forces underlying mitochondrial genome evolution. PLoS Genet 8:1002876. https://doi.org/10.1371/journal.pgen.1002876
Bjelland T, Grube M, Hoem S, Jorgensen SL, Daae FL, Thorseth IH, Øvreås L (2011) Microbial metacommunities in the lichen–rock habitat. Environ Microbiol 3:434–442. https://doi.org/10.1111/j.1758-2229.2010.00206.x
Bullerwell CE, Gray MW (2004) Evolution of the mitochondrial genome, protist connections to animals, fungi and plants. Curr Opin Microbiol 7:528–534. https://doi.org/10.1016/j.mib.2004.08.008
Chagnon PL, Magain N, Miadlikowska J, Lutzoni F (2019) Species diversification and phylogenetically constrained symbiont switching generated high modularity in the lichen genus Peltigera. J Ecol 107(4):1645–1661. https://doi.org/10.1111/1365-2745.13207
Dal Grande F, Meiser A, Tzovaras BG, Jürgen OTTE, Ebersberger I, Schmitt I (2018) The draft genome of the lichen-forming fungus Lasallia hispanica (Frey) Sancho & A. Crespo. Lichenologist 50:329–340. https://doi.org/10.1017/S002428291800021X
Darling AC, Mau B, Blattner FR, Perna NT (2004) Mauve, multiple alignment of conserved genomic sequence with rearrangements. Genome Res 14:1394–1403. https://doi.org/10.1101/gr.2289704
Dierckxsens N, Mardulyn P, Smits G (2017) NOVOPlasty: de novo assembly of organelle genomes from whole genome data. Nucleic Acids Res 45:e18–e18. https://doi.org/10.1093/nar/gkw955
Drew EA, Smith DC (1967) Studies in the physiology of lichens. VII. The physiology of the nostoc symbiont of Peltigera polydactyla compared with cultured and free-living forms. New Phytol 66(3):379–388. https://doi.org/10.1111/j.1469-8137.1967.tb06017.x
Goward T, Goffinet B (2000) Peltigera chionophila, a new lichen (Ascomycetes) from the Western Cordillera of North America. Bryologist 493–498. https://doi.org/10.2307/3244136
Gray MW, Burger G, Lang BF (1999) Mitochondrial evolution. Science 283:1476–1481. https://doi.org/10.1126/science.283.5407.1476
Greshake B, Zehr S, Dal Grande F, Meiser A, Schmitt I, Ebersberger I (2016) Potential and pitfalls of eukaryotic metagenome skimming: a test case for lichens. Mol Ecol Resour 16:511–523. https://doi.org/10.1111/1755-0998.12463
Hejnol A, Obst M, Stamatakis A, Ott M, Rouse GW, Edgecombe GD, Dunn CW (2009) Assessing the root of bilaterian animals with scalable phylogenomic methods. Proc Royal Soc B 276:4261–4270. https://doi.org/10.1098/rspb.2009.0896
Huelsenbeck JP, Ronquist F (2001) MRBAYES, Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755. https://doi.org/10.1093/bioinformatics/17.8.754
Kalyaanamoorthy S, Minh BQ, Wong T, Haeseler AV, Jermiin LS (2017) Modelfinder: fast model selection for accurate phylogenetic estimates. Nat Methods 14:587–589. https://doi.org/10.1038/nmeth.4285
Katoh K, Rozewicki J, Yamada KD (2019) MAFFT online service, multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform 20(4):1160–1166. https://doi.org/10.1093/bib/bbx108
Keepers KG, Pogoda CS, White KH, Anderson-Stewart CR, Tripp EA (2019) Whole genome shotgun sequencing detects greater lichen fungal diversity than amplicon-based methods in environmental samples. Front Ecol Evol 7:484. https://doi.org/10.3389/fevo.2019.00484
Kitazaki K, Kubo T (2010) Cost of having the largest mitochondrial genome, evolutionary mechanism of plant mitochondrial genome. J Bot. https://doi.org/10.1155/2010/620137
Klos A, Rajfur M, Šrámek I, Waclawek M (2011) Use of lichen and moss in assessment of forest contamination with heavy metals in Praded and Glacensis Euroregions (Poland and Czech Republic). Water Air Soil Pollut 222:367–376. https://doi.org/10.1007/s11270-011-0830-9
Larson DW (1987) The absorption and release of water by lichens. Biblioth Lichenol 25:351–360
Leavitt SD, Grewe F, Widhelm T, Muggia L, Wray B, Lumbsch HT (2016) Resolving evolutionary relationships in lichen-forming fungi using diverse phylogenomic datasets and analytical approaches. Sci Rep 6:22262. https://doi.org/10.1038/srep22262
Lendemer JC, Anderson F (2012) Molecular data confirm the identity of populations of the water fan lichen from eastern Canada as Peltigera hydrothyria s. str. Opusc Philolichenum 11:139–140
Liu Y, Xue JY, Wang B, Li L, Qiu YL (2011) The mitochondrial genomes of the early land plants Treubia lacunosa and Anomodon rugelii, dynamic and conservative evolution. PLoS ONE 6(10):e25836. https://doi.org/10.1371/journal.pone.0025836
Luo H, Wei X, Yamamoto Y, Liu Y, Wang L, Jung JS, Koh YJ, Hur JS (2010) Antioxidant activities of edible lichen Ramalina conduplicans and its free radical-scavenging constituents. Mycoscience 51:391–395. https://doi.org/10.1007/S10267-010-0048-5
Lynch M, Koskella B, Schaack S (2006) Mutation pressure and the evolution of organelle genomic architecture. Science 311:1727–1730. https://doi.org/10.1126/science.1118884
Magain N, Sérusiaux E, Zhurbenko MP, Lutzoni F, Miadlikowska J (2016) Disentangling the Peltigera polydactylon species complex by recognizing two new taxa, P. polydactylon subsp. udeghe and P. seneca. Herzogia 29:514–528
Magain N, Miadlikowska J, Goffinet B, Serusiaux E, Lutzoni F (2017a) Macroevolution of specificity in cyanolichens of the genus Peltigera section Polydactylon (Lecanoromycetes, Ascomycota). Syst Biol 66:74–99. https://doi.org/10.1093/sysbio/syw065
Magain N, Miadlikowska J, Mueller O, Gajdeczka M, Truong C, Salamov AA, Lutzoni F (2017b) Conserved genomic collinearity as a source of broadly applicable, fast evolving, markers to resolve species complexes: a case study using the lichen-forming genus Peltigera section Polydactylon. Mol Phylogenet Evol 117:10–29. https://doi.org/10.1016/j.ympev.2017.08.013
Magain N, Truong C, Goward T, Niu D, Goffinet B, Sérusiaux E, Vitikainen O, Lutzoni F, Miadlikowska J (2018) Species delimitation at a global scale reveals high species richness with complex biogeography and patterns of symbiont association in Peltigera section Peltigera (lichenized Ascomycota: Lecanoromycetes). Taxon 67:836–870
Meiser A, Otte J, Schmitt I, Grande FD (2017) Sequencing genomes from mixed DNA samples-evaluating the metagenome skimming approach in lichenized fungi. Sci Rep 7:1–13. https://doi.org/10.1038/s41598-017-14576-6
Miadlikowska J, Lutzoni F (2000) Phylogenetic revision of the genus Peltigera (lichen-forming Ascomycota) based on morphological, chemical, and large subunit nuclear ribosomal DNA data. Int J Plant Sci 161(6):925–958
Miadlikowska J, Richardson D, Magain N (2014) Phylogenetic placement, species delimitation, and cyanobiont identity of endangered aquatic Peltigera species (lichen-forming Ascomycota, Lecanoromycetes). Am J Bot 101(7):1141–1156. https://doi.org/10.3732/ajb.1400267
Miadlikowska J, Magain N, Pardo de la Hoz C, Niu D, Goward T, Sérusiaux E, Lutzoni F (2018) Species in section Peltidea (aphthosa group) of the genus Peltigera remain cryptic after molecular phylogenetic revision. Plant Fungal Syst 63(2). https://doi.org/10.2478/pfs-2018-0007
Michael T, Pascal L, Tommaso P, Ulbricht-Jones ES, Axel F, Ralph B, Stephan G (2017) Geseq-versatile and accurate annotation of organelle genomes. Nucleic Acids Res 5:W6–W11. https://doi.org/10.1093/nar/gkx391
Mohanta TK, Bae H (2015) The diversity of fungal genome. Biol Proced Online 17:1–9. https://doi.org/10.1186/s12575-015-0020-z
Nash HT (1996) Lichen biology. Cambridge University Press, Cambridge, England
Oksanen I (2006) Ecological and biotechnological aspects of lichens. Appl Microbiol Biotechnol 73:723–734. https://doi.org/10.1007/s00253-006-0611-3
Palmer JD, Adams KL, Cho Y, Parkinson CL, Qiu YL, Song K (2000) Dynamic evolution of plant mitochondrial genomes: mobile genes and introns and highly variable mutation rates. Proc Natl Acad Sci USA 97:6960–6966. https://doi.org/10.1073/pnas.97.13.6960
Pizarro D, Divakar PK, Grewe F, Leavitt SD, Huang JP, Dal Grande F, Lumbsch HT (2018) Phylogenomic analysis of 2556 single-copy protein-coding genes resolves most evolutionary relationships for the major clades in the most diverse group of lichen-forming fungi. Fungal Divers 92(1):31–41. https://doi.org/10.1007/s13225-018-0407-7
Pogoda CS, Keepers KG, Nadiadi AY, Bailey DW, Lendemer JC, Tripp EA, Kane NC (2019) Genome streamlining via complete loss of introns has occurred multiple times in lichenized fungal mitochondria. Ecol Evol 1–19. https://doi.org/10.1002/ece3.5056
Qiu YL, Li L, Wang B, Chen Z, Knoop V, Groth-Malonek M, Dombrovska O, Lee J, Kent L, Rest J (2006) The deepest divergences in land plants inferred from phylogenomic evidence. Proc Natl Acad Sci 103:15511–15516. https://doi.org/10.1073/pnas.0603335103
Reis MD, Inoue J, Hasegawa M, Asher RJ, Donoghue P, Yang Z (2012) Phylogenomic datasets provide both precision and accuracy in estimating the timescale of placental mammal phylogeny. Proc Biol 279:3491–3500. https://doi.org/10.1098/rspb.2012.0683
Rocha EPC (2003) DNA repeats lead to the accelerated loss of gene order in bacteria. Trends Genet 19:600–603. https://doi.org/10.1016/j.tig.2003.09.011
Rokas A, Ladoukakis E, Zouros E (2003) Animal mitochondrial DNA recombination revisited. Trends Ecol Evol 18:411–417. https://doi.org/10.1016/S0169-5347(03)00125-3
Rozas J, Ferrer-Mata A, Sánchez-DelBarrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE, Sánchez-Gracia A (2017) DnaSP 6, DNA sequence polymorphism analysis of large data sets. Mol Biol Evol 34(12):3299–3302. https://doi.org/10.1093/molbev/msx248
Simon A, Liu Y, Sérusiaux E, Goffinet B (2017) Complete mitogenome sequence of Ricasolia amplissima (Lobariaceae) reveals extensive mitochondrial DNA rearrangement within the Peltigerales (lichenized ascomycetes). Bryologist 120:335–339. https://doi.org/10.1639/0007-2745-120.3.335
Smith DC, Drew EA (1965) Studies in the physiology of lichens: V. Translocation from the algal layer to the medulla in Peltigera Polydactyla. New Phytol 64(2):195–200
Stefan K, Choudhuri JV, Enno O, Chris S, Jens S, Robert G (2001) Reputer: the manifold applications of repeat analysis on a genomic scale. Nucleic Acids Res 22:4633–4642. https://doi.org/10.1093/nar/29.22.4633
Sudhir K, Glen S, Koichiro T (2016) Mega7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 7:1870. https://doi.org/10.1093/molbev/msw054
Spribille T, Tuovinen V, Resl P, Vanderpool D, Wolinski H, Aime MC, McCutcheon JP (2016) Basidiomycete yeasts in the cortex of ascomycete macrolichens. Science 353(6298):488–492. https://doi.org/10.1126/science.aaf8287
Wei XL, Wang XY, Koh YJ, Hur JS (2009) Taxonomic study of Peltigera (Peltigeraceae, Ascomycota) in Korea. Mycobiology 37(3):189–196
Wu M, Eisen JA (2008) A simple, fast, and accurate method of phylogenomic inference. Genome Biol Evol 9:R151. https://doi.org/10.1186/gb-2008-9-10-r151
Xavier BB, Miao VP, Jónsson ZO, Andresson OS (2012) Mitochondrial genomes from the lichenized fungi Peltigera membranacea and Peltigera malacea: features and phylogeny. Fungal Biol 802–814. https://doi.org/10.1016/j.funbio.2012.04.013
Zhao Y, Wang M, Xu B (2021) A comprehensive review on secondary metabolites and health-promoting effects of edible lichen. J Funct Foods 104283. https://doi.org/10.1016/j.jff.2020.104283
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The authors would like to thank anonymous reviewers for helpful comments.
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This work was jointly funded by the National Natural Science Foundation of China (31760052, 32160046) and Natural Science Foundation of Xinjiang Province (2022D03005, 2021D01C061).
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Reyim Mamut designed this study and completed the manuscript; Gulmira Anwar participated in data analysis; Lidan Wang and Jinjin Fang conducted the experiment. All authors read and approved the final manuscript.
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Mamut, R., Anwar, G., Wang, L. et al. The mitogenomes characterization of two Peltigera species (Peltigera elisabethae and Peltigera polydactylon) and comparative mitogenomic analyses of six Peltigera. J Appl Genetics 64, 819–829 (2023). https://doi.org/10.1007/s13353-023-00791-7
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DOI: https://doi.org/10.1007/s13353-023-00791-7