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Novel rearrangements in the mitochondrial genomes of the Ceramiales (Rhodophyta) and evolutionary implications

  • Min Ho Seo (Department of Biological Sciences, Sungkyunkwan University) ;
  • Shin Chan Kang (Department of Biological Sciences, Sungkyunkwan University) ;
  • Kyeong Mi Kim (Department of Taxonomy and Systematics, National Marine Biodiversity Institute of Korea) ;
  • Min Seok Kwak (Department of Taxonomy and Systematics, National Marine Biodiversity Institute of Korea) ;
  • Jihoon Jo (Department of Biological Sciences, Sungkyunkwan University) ;
  • Han-Gu Choi (Division of Life Sciences, Korea Polar Research Institute) ;
  • Ga Hun Boo (Department of Biological Sciences, Sungkyunkwan University) ;
  • Hwan Su Yoon (Department of Biological Sciences, Sungkyunkwan University)
  • 투고 : 2023.10.30
  • 심사 : 2023.12.02
  • 발행 : 2023.12.21

초록

The Ceramiales is the most diverse and species-rich group (2,669 spp.) of red algae, and it is widely distributed from tropical to polar oceans. Mitochondrial genomes (mitogenomes) and other genes have contributed to our knowledge regarding the classification and phylogeny of this diverse red algal group; however, the mitogenome architecture remains understudied. Here, we compared 42 mitogenomes, including 19 newly generated in this study, to expand our knowledge. The number of genes in mitogenome varied from 43 to 68 due to gene duplication. The mitogenome architecture was also variable, categorized into four types (A-D): type A = ancestral type with a basic composition; type B = those with inverse transpositions; type C = those with inverted duplications; and type D = those with both inversion and duplication. The palindromic and inverted repeats were consistently found in flanking regions of the rearrangement, especially near the cob and nad6 genes. The three rearranged mitogenome architectures (types B, C, D) are the first report of these in red algae. Phylogenetic analyses of 23 protein-coding genes supported the current familial classification of the Ceramiales, implying that the diversity of mitogenome architecture preceded the phylogenetic relationships. Our study suggests that palindromic and inverted repeats may drive mitogenome architectural variation.

키워드

과제정보

We thank to Robert A. Andersen for reading and providing valuable corrections in the first version of the manuscript. This work was supported by grants from the National Research Foundation of Korea (grant number NRF-2021R1I1A1A01049542, 2022R1A2B5B03002312, 20-22R1A5A1031361), the Cooperative Research Program for Agriculture Science and Technology Development (Project No. RS-2023-00231243), Rural Development Administration, Republic of Korea, and National Marine Biodiversity Institute of Korea Program (2023M00200).

참고문헌

  1. Achaz, G., Coissac, E., Netter, P. & Rocha, E. P. C. 2003. Associations between inverted repeats and the structural evolution of bacterial genomes.  Genetics  164:1279-1289. Amos, D., Aguilar, V., Barber-Scott, K., Bustamante, D. E.,  https://doi.org/10.1093/genetics/164.4.1279
  2. Calderon, M. S., Carrasco, R., Carrion, J. V., Castro, N., Celso, D., Cedillo, S. M. C., Cortes, R., Dao, L., De Santos, S., Ebie, Z., Evangelista, L., Fernandez, S. L., Flores, G., Garcia, L., Gonzalez, E., Hernandz, A., Hernandez, M. O., Hughey, J. R., Luna, L., Marquez, K., Martinez, V., Mendoza, J. E., Mirassou, L., Murillo, C., Parr, M. Jr., Perez, J., Perez-Santana, I., Perez, H., Quezada, A., Quizon, S., Sandberg, S., Santos, A., Tapia, J., Tineo, D. & Vang, M. N. 2021. Transfer of the marine red alga Erythrocystis saccata (Rhodomelaceae, Rhodophyta) to the tribe Streblocladieae inferred from organellar genome analysis. Phytotaxa 507:266-270.  https://doi.org/10.11646/phytotaxa.507.3.4
  3. Barros-Barreto, M. B., Jaramillo, M. A., Hommersand, M. H., Ferreira, P. C. G. & Maggs, C. A. 2023. Phylogenetic analysis of the red algal tribe Ceramieae reveals multiple morphological homoplasies but defines new genera. Cryptogam. Algol. 44:13-58. 
  4. Beck, N. & Lang, B. F. 2010. MFannot, organelle genome annotation websever. Available from: https://github.com/BFL-lab/Mfannot. Accessed Sep 1, 2023. 
  5. Bolger, A. M., Lohse, M. & Usadel, B. 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114-2120.  https://doi.org/10.1093/bioinformatics/btu170
  6. Boo, G. H., Hughey, J. R., Miller, K. A. & Boo, S. M. 2016. Mitogenomes from type specimens, a genotyping tool for morphologically simple species: ten genomes of agarproducing red algae. Sci. Rep. 6:35337. 
  7. Boo, G. H., Zubia, M., Hughey, J. R., Sherwood, A. R., Fujii, M. T., Boo, S. M. & Miller, K. A. 2020. Complete mitochondrial genomes reveal population-revel patterns in the widespread red alga Gelidiella fanii (Gelidiales, Rhodophyta). Front. Mar. Sci. 7:583957. 
  8. Brazda, V., Kolomaznik, J., Lysek, J., Haronikova, L., Coufal, J. & St'astny, J. 2016. Palindrome analyser: a new webbased server for predicting and evaluating inverted repeats in nucleotide sequences. Biochem. Biophys. Res. Commun. 478:1739-1745.  https://doi.org/10.1016/j.bbrc.2016.09.015
  9. Carvalho, C. M. B., Ramocki, M. B., Pehlivan, D., Franco, L. M., Gonzaga-Jauregui, C., Fang, P., McCall, A., Pivnick, E. K., Hines-Dowell, S., Seaver, L. H., Friehling, L., Lee, S., Smith, R., Del Gaudio, D., Withers, M., Liu, P., Cheung, S. W., Belmont, J. W., Zoghbi, H. Y., Hastings, P. J. & Lupski, J. R. 2011. Inverted genomic segments and complex triplication rearrangements are mediated by inverted repeats in the human genome. Nat. Genet. 43:1074-1081.  https://doi.org/10.1038/ng.944
  10. Castresana, J. 2000. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol. Biol. Evol. 17:540-552.  https://doi.org/10.1093/oxfordjournals.molbev.a026334
  11. Cho, C. H., Park, S. I., Ciniglia, C., Yang, E. C., Graf, L., Bhattacharya, D. & Yoon, H. S. 2020. Potential causes and consequences of rapid mitochondrial genome evolution in thermoacidophilic Galdieria (Rhodophyta). BMC Evol. Biol. 20:112. 
  12. Choi, H.-G., Kraft, G. T., Kim, H.-S., Guiry, M. D. & Saunders, G. W. 2008. Phylogenetic relationships among lineages of the Ceramiaceae (Ceramiaes, Rhodophyta) based on nuclear small subunit rDNA sequence data. J. Phycol. 44:1033-1048.  https://doi.org/10.1111/j.1529-8817.2008.00554.x
  13. Choi, H.-G., Kraft, G., Lee, I. K. & Saunders, G. 2002. Phylogenetic analyses of anatomical and nuclear SSU rDNA sequence data indicate that the Dasyaceae and Delesseriaceae (Ceramiales, Rhodophyta) are polyphyletic. Eur. J. Phycol. 37:551-569.  https://doi.org/10.1017/S0967026202003967
  14. Cunningham, L. A., Cote, A. G., Cam-Ozdemir, C. & Lewis, S. M. 2003. Rapid, stabilizing palindrome rearrangements in somatic cells by the center-break mechanism.  Mol. Cell Biol. 23:8740-8750.  https://doi.org/10.1128/MCB.23.23.8740-8750.2003
  15. Diaz-Tapia, P., Maggs, C. A., West, J. A. & Verbruggen, H. 2017. Analysis of chloroplast genomes and supermatrix inform reclassification of the Rhodomelaceae (Rhodophyta). J. Phycol. 53:920-937.  https://doi.org/10.1111/jpy.12553
  16. Diaz-Tapia, P., Pasella, M. M., Verbruggen, H. & Maggs, C. A. 2019. Morphological evolution and classification of the red algal order Ceramiales inferred using plastid phylogenomics. Mol. Phylogenet. Evol. 137:76-85.  https://doi.org/10.1016/j.ympev.2019.04.022
  17. Diaz-Tapia, P., Rodriguez-Bujan, I., Maggs, C. A. & Verbruggen, H. 2023. Phylogenomic analysis of pseudocryptic diversity reveals the new genus Deltalsia (Rhodomelaceae, Rhodophyta). J. Phycol. 59:264-276.  https://doi.org/10.1111/jpy.13311
  18. Dierckxsens, N., Mardulyn, P. & Smits, G. 2017. NOVOPlasty: de novo assembly of organelle genomes from whole genome data. Nucleic Acids Res. 45:e18. 
  19. Doyle, J. J. & Doyle, J. L. 1987. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem. Bull. 19:11-15. 
  20. Guiry, M. D. & Guiry, G. M. 2023. Algae Base. World-wide electronic publication, National University of Ireland, Galway. Available from: http://www.algaebase.org. Accessed Sep 15, 2023. 
  21. Hommersand, M. H. 1963. The morphology and classification of some Ceramiaceae and Rhodomelaceae. Univ. Calif. Publ. Bot. 35:165-366. 
  22. Hughey, J. R. & Boo, G. H. 2016. Genomic and phylogenetic analysis of Ceramium cimbricum (Ceramiales, Rhodophyta) from the Atlantic and Pacific oceans supports the naming of a new invasive Pacific entity Ceramium sungminbooi sp. nov. Bot. Mar. 59:211-222.  https://doi.org/10.1515/bot-2016-0036
  23. Hughey, J. R., Gabrielson, P. W., Rohmer, L., Tortolani, J., Silva, M., Miller, K. A., Young, J. D., Martell, C. & Ruediger, E. 2014. Minimally destructive sampling of type specimens of Pyropia (Bangiales, Rhodophyta) recovers complete plastid and mitochondrial genomes. Sci. Rep. 4:5113. 
  24. Hughey, J. R. & Miller, K. A. 2021. Genetic investigation of three type specimens of Osmundea (Rhodomelaceae, Rhodophyta) from the Gulf of California, Mexico and California, USA. Phytotaxa 489:65-78.  https://doi.org/10.11646/phytotaxa.489.1.5
  25. Huisman, J. 2018. Algae of Australia. 2. Red algae. ABRS & CISRO Publishing, Canberra, 672 pp. 
  26. Iha, C., Grassa, C. J., Lyra, G. M., Davis, C. C., Verbruggen, H. & Oliveira, M. C. 2018. Organellar genomes: a useful tool to study evolutionary relationships and molecular evolution and Gracilariaceae (Rhodophyta). J. Phycol. 54:775-787.  https://doi.org/10.1111/jpy.12765
  27. Jiang, Z., Li, R., Cui, Y., Jia, X., Liu, T., Wang, X. & Qu, J. 2021. The complete mitochondrial genome and phylogenetic analysis of Neorhodomela munita. Mitochondrial DNA B Resour. 6:2746-2747. 
  28. Jin, J.-J., Yu, W.-B., Yang, J.-B., Song, Y., dePamphilis, C. W., Yi, T.-S. & Li, D.-Z. 2020. GetOrganelle: a fast and versatile toolkit for accurate de novo assembly of organelle genomes. Genome Biol. 21:241. 
  29. Kylin, H. 1956. Die Gattungen der Rhodophyceen. C.W.K. Gleerups, Lund, 673 pp. 
  30. Langmead, B. & Salzberg, S. L. 2012. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9:357-359.  https://doi.org/10.1038/nmeth.1923
  31. Lee, J.-M., Boo, S. M., Mansilla, A. & Yoon, H. S. 2015. Unique repeat and plasmid sequences in the mitochondrial genome of Gracilaria chilensis (Gracilariales, Rhodophyta). Phycologia 54:20-23.  https://doi.org/10.2216/PH14-97.1
  32. Lee, J. M., Song, H. J., Park, S. I., Lee, Y. M., Jeong, S. Y., Cho, T. O., Kim, J. H., Choi, H.-G., Choi, C. G., Nelson, W. A., Fredericq, S., Bhattacharya, D. & Yoon, H. S. 2018. Mitochondrial and plastid genomes from coralline algae provide insights into the incongruent evolutionary histories of organelles. Genome Biol. Evol. 10:2961-2972.  https://doi.org/10.1093/gbe/evy222
  33. Lee, Y., Cho, C. H., Noh, C., Yang, J. H., Park, S. I., Lee, Y. M., West, J. A., Bhattacharya, D., Jo, K. & Yoon, S. H. 2023. Origin of minicircular mitochondrial genomes in red algae. Nat. Commun. 14:3363. 
  34. Lin, S.-M., Fredericq, S. & Hommersand, M. H. 2001. Systematics of the Delesseriaceae (Ceramiales, Rhodophyta) based on large subunit rDNA and rbcL sequences, including the Phycodryoideae, subfam. nov. J. Phycol. 37:881-899.  https://doi.org/10.1046/j.1529-8817.2001.01012.x
  35. Lowe, T. M. & Chan, P. P. 2016. tRNAscan-SE on-line: integrating search and context for analysis of transfer RNA genes. Nucleic Acids Res. 44:W54-W57.  https://doi.org/10.1093/nar/gkw413
  36. Maggs, C. A. & Hommersand, M. H. 1993. Seaweeds of the British Isles. Vol. 1. Rhodophyta. Part 3A. Ceramiales. Natural History Museum, London, 444 pp. 
  37. Miklenic, M. S. & Svetec, I. K. 2021. Palindromes in DNA: a risk for genome stability and implications in cancer. Int. J. Mol. Sci. 22:2840. 
  38. Minh, B. Q., Schmidt, H. A., Chernomor, O., Schrempf, D., Woodhams, M. D., von Haeseler, A. & Lanfear, R. 2020. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol. Biol. Evol. 37:1530-1534.  https://doi.org/10.1093/molbev/msaa015
  39. Ranwez, V., Douzery, E. J., Cambon, C., Chantret, N. & Delsuc, F. 2018. MACSE v2: toolkit for the alignment of coding sequences accounting for frameshifts and stop codons. Mol. Biol. Evol. 35:2582-2584.  https://doi.org/10.1093/molbev/msy159
  40. Reams, A. B. & Roth, J. R. 2015. Mechanisms of gene duplication and amplification. Cold Spring Harb. Perspect. Biol. 7:a016592. 
  41. Salomaki, E. D. & Lane, C. E. 2017. Red algal mitochondrial genomes are more complete than previously reported. Genome Biol. Evol. 9:48-63. 
  42. Tamayo, D. A. & Hughey, J. R. 2016. Organellar genome analysis of the marine red alga Dasya binghamiae (Dasyaceae, Rhodophyta) reveals an uncharacteristic florideophyte mitogenome structure. Mitochondrial DNA Part B Resour. 1:510-511.  https://doi.org/10.1080/23802359.2016.1192515
  43. Wick, R. R., Schultz, M. B., Zobel, J. & Holt, K. E. 2015. Bandage: interactive visualization of de novo genome assemblies. Bioinformatics 31:3350-3352.  https://doi.org/10.1093/bioinformatics/btv383
  44. Witte, C. P., Le, Q. H., Bureau, T. & Kumar, A. 2001. Terminalrepeat retrotransposons in miniature (TRIM) are involved in restructuring plant genomes. Proc. Natl. Acad. Sci. U. S. A. 98:13778-13783.  https://doi.org/10.1073/pnas.241341898
  45. Womersley, H. B. S. 1998. The marine benthic flora of southern Australia - Part IIIC. Ceramiales - Ceramiaceae, Dasyaceae. Australian Biological Resources Study & State Herbarium of South Australia, Canberra & Adelaide, 535 pp. 
  46. Wynne, M. J. & Schneider, C. W. 2023. Reinstatement of Ceramothamnion H. Richards (1901), a replacement name for the newly described Stirkia (Ceramiaceae, Rhodophyta). Not. Algarum 296:1-4. 
  47. Yang, E. C., Kim, K. M., Kim, S. Y., Lee, J., Boo, G. H., Lee, J. -H., Nelson, W. A., Yi, G., Schmidt, W. E., Fredericq, S., Boo, S. M., Bhattacharya, D. & Yoon, H. S. 2015. Highly conserved mitochondrial genomes among multicellular red algae of the Florideophyceae. Genome Biol. Evol. 7:2394-2406.  https://doi.org/10.1093/gbe/evv147