Skip to main content Skip to main navigation menu Skip to site footer
Articles
Published: 2021-06-30

The mitochondrial genomes of bryophytes

Laboratory of Southern Subtropical Plant Diversity, Fairy Lake Botanical Garden, Shenzhen & Chinese Academy of Sciences, Shenzhen 518004, China
Laboratory of Southern Subtropical Plant Diversity, Fairy Lake Botanical Garden, Shenzhen & Chinese Academy of Sciences, Shenzhen 518004, China
Bryophytes mitochondrial genomes gene content introns recombination

Abstract

In contrast to the highly variable mitogenomes of vascular plants, the composition and architecture of mitogenomes within the three bryophyte lineages appear stable and invariant. Currently, complete mitogenomes are available from 113 bryophyte accessions of 71 genera and 28 orders. Liverworts and mosses hold a rich mitochondrial (mt) gene repertoire among land plants with 40–42 protein-coding genes, whereas hornworts maintain the smallest functional gene set among land plants, of only around two dozen protein-coding genes, with the majority of ribosomal genes pseudogenized and all cytochrome c maturase genes lost. The rRNA and tRNA genes are also conserved and rich in mosses and liverworts, whereas subject to patchy losses in hornworts. In contrast to the conserved gene set, intron content varies significantly with only one intron shared among the three bryophyte lineages. Bryophytes hold relatively compact mitogenomes with narrow size fluctuations. Among the three bryophyte lineages, intergenic spacers and repeat content are smallest in mosses, largest in hornworts, and intermediate in liverworts, mirroring their size differences and levels of structural dynamics among the three lineages. Mosses, with the least repeated sequences, show the most static genome structure; whereas hornworts, with a relatively large set of repeated sequences, experience 1–4 rearrangements; liverworts, with intermediate repeat levels, see only one structural variant that requires two inversions to gain collinearity with the mitogenome of other liverworts. Repeat sequences were evoked to explain the mt gene order rearrangements in hornwort and liverwort mitogenomes; with the latter also supported by sequencing read evidence, which suggests that the conserved mitogenome structure observed in bryophyte lineages might be shaped by low repeat recombination level, and/or along with the intensified nucleus’ surveillance. Mitochondrial RNA editing is abundant in hornworts, with medium frequency and high variation in liverwort species, and generally limited in mosses, reflecting the diversity of nuclear encoded PPR proteins that are functionally related to RNA editing processes.

References

  1. Alverson, A.J., Wei, X.X., Rice, D.W., Stern, D.B., Barry, K. & Palmer, J.D. (2010) Insights into the evolution of mitochondrial genome size from complete sequences of Citrullus lanatus and Cucurbita pepo (Cucurbitaceae). Molecular Biology & Evolution 27: 1436. https://doi.org/10.1093/molbev/msq029

  2. André, C., Levy, A. & Walbot, V. (1992) Small repeated sequences and the structure of plant mitochondrial genomes. Trends in Genetics 8: 128–132.  https://doi.org/10.1016/0168-9525(92)90370-J

  3. Bell, D., Lin, Q., Gerelle, W.K., Joya, S., Chang, Y., Taylor, Z.N., Rothfels, C.J., Larsson, A., Villarreal, J.C., Li, F.W., Pokorny, L., Szovenyi, P., Crandall-Stotler, B., DeGironimo, L., Floyd, S.K., Beerling, D.J., Deyholos, M.K., von Konrat, M., Ellis, S., Shaw A.J., Chen, T., Wong, G.K., Stevenson, D.W., Palmer, J.D. & Graham, S.W. (2020) Organellomic data sets confirm a cryptic consensus on (unrooted) land-plant relationships and provide new insights into bryophyte molecular evolution. American Journal of Botany 107: 91–115. https://doi.org/10.1002/ajb2.1397

  4. Bennetzen, J.L. (2000) Transposable element contributions to plant gene and genome evolution. Plant Molecular Biology 42: 251–269. https://doi.org/10.1023/A:1006344508454

  5. Bentolila, S., Heller, W.P., Sun, T., Babina, A.M., Friso, G., Wijk, K.J.V. & Hanson, M.R. (2012) Rip1, a member of an arabidopsis protein family, interacts with the protein RARE1 and broadly affects RNA editing. Proceedings of the National Academy of Sciences of The United States of America 109: 8372–8373. https://doi.org/10.1073/pnas.1121465109

  6. Burger, G., Gray, M.W. & Lang, B.F. (2003) Mitochondrial genomes: Anything goes. Trends in Genetics 19: 709–716. https://doi.org/10.1016/j.tig.2003.10.012

  7. Cheng, S., Xian, W., Fu, Y., Marin, B., Keller, J., Wu, T., Sun, W., Li, X., Xu, Y., Zhang, Y., Wittek, S., Reder, T., Gunther, G., Gontcharov, A., Wang, S., Li, L., Liu, X., Wang, J., Yang, H., Xu, X., Delaux, P.M., Melkonian, B., Wong, G.K. & Melkonian, M. (2019) Genomes of subaerial Zygnematophyceae provide insights into land plant evolution. Cell 179: 1057–1067. https://doi.org/10.1016/j.cell.2019.10.019

  8. Covello, P.S. & Gray, M.W. (1993) On the evolution of RNA editing. Trends in Genetics 9: 265–268. https://doi.org/10.1016/0168-9525(93)90011-6

  9. Csuos, M. (2010) Count: Evolutionary analysis of phylogenetic profiles with parsimony and likelihood. Bioinformatics 26: 1910–1912. https://doi.org/10.1093/bioinformatics/btq315

  10. Darracq, A., Varre, J.S. & Touzet, P. (2010) A scenario of mitochondrial genome evolution in maize based on rearrangement events. BMC Genomics 11: 233. https://doi.org/10.1186/1471-2164-11-233

  11. Dong, S., Xue, J.Y., Zhang, S., Li, Z., Hong, W., Chen, Z.D., Goffinet, B. & Liu, Y. (2018a) Complete mitochondrial genome sequence of Anthoceros angustus: Conservative evolution of the mitogenomes in hornworts. The Bryologist 121: 14–22. https://doi.org/10.1639/0007-2745-121.1.014

  12. Dong, S., Zhao, C., Fei, C., Liu, Y., Zhang, S., Hong, W., zhang, L. & Liu, Y. (2018b) The complete mitochondrial genome of the early flowering plant Nymphaea colorata is highly repetitive with low recombination. BMC Genomics 19: 614. https://doi.org/10.1186/s12864-018-4991-4

  13. Dong, S., Zhao, C., Zhang, S., Zhang, L., Wu, H., Liu, H., Goffinet, B. & Liu, Y. (2019a) Mitochondrial genomes of the early land plant lineage liverworts (Marchantiophyta): Conserved genome structure, and ongoing low frequency recombination. BMC Genomics 20: 953. https://doi.org/10.1186/s12864-019-6365-y

  14. Dong, S., Zhao, C., Zhang, S., Wu, H., Mu, W., Wei, T., Li, N., Wan, T., Liu, H., Cui, J., Zhu, R., Goffinet, B. & Liu, Y. (2019b) The amount of RNA editing sites in liverwort organellar genomes is correlated with the GC content and PPR protein diversity. Genome Biology & Evolution 11: 3233–3239. https://doi.org/10.1093/gbe/evz232

  15. Duff, R.J. & Moore, F.B.G. (2005) Pervasive RNA editing among hornwort rbcL transcripts except Leiosporoceros. Journal of Molecular Evolution 61: 571–578. https://doi.org/10.1007/s00239-004-0146-0

  16. Edera, A.A., Gandini, C.L. & Sanchez-Puerta, M.V. (2018) Towards a comprehensive picture of C-to-U RNA editing sites in angiosperm mitochondria. Plant Molecular Biology 97: 215–231. https://doi.org/10.1007/s11103-018-0734-9

  17. Frangedakis, E., Shimamura, M., Villarreal, J.C., Li, F.W., Tomaselli, M., Waller, M., Sakakibara, K., Renzaglia, K.S. & Szvényi, P. (2020) The Hornworts: Morphology, evolution and development. New Phytologist 229 (2): 735–754. https://doi.org/10.1111/nph.16874

  18. Gerke, P., Szövényi, P., Neubauer, P., Lenz, H., Gutmann, B., McDowell, R., Small, I., Schallenberg‐Rüdinger, M. & Knoop, V. (2019) Towards a plant model for enigmatic U‐to‐C RNA editing: the organelle genomes, transcriptomes, editomes and candidate RNA editing factors in the hornwort Anthoceros agrestis. New Phytologist 225 (5): 1974–1992. https://doi.org/10.1111/nph.16297

  19. Gitzendanner, M.A., Soltis, P.S., Wong, G.K.S., Ruhfel, B.R. & Soltis, D.E. (2018) Plastid phylogenomic analysis of green plants: A billion years of evolutionary history. American Journal of Botany 105: 291–301. https://doi.org/10.1002/ajb2.1048

  20. Goffinet, B. & Shaw, A.J. (2009) Bryophyte biology. 2nd ed. Cambridge: Cambridge University Press. https://doi.org/10.1017/CBO9780511754807

  21. Grewe, F., Herres, S., Viehover, P., Polsakiewicz, M., Weisshaar, B. & Knoop, V. (2011) A unique transcriptome: 1782 positions of RNA editing alter 1406 codon identities in mitochondrial mRNAs of the lycophyte Isoetes engelmannii. Nucleic Acids Research 39: 2890–2902. https://doi.org/10.1093/nar/gkq1227

  22. Guo, W., Zhu, A., Fan, W. & Mower, J.P. (2017) Complete mitochondrial genomes from the ferns Ophioglossum californicum and Psilotum nudum are highly repetitive with the largest organellar introns. New Phytologist 213: 391–403. https://doi.org/10.1111/nph.14135

  23. Guo, X., Zhang, Z., Gerstein, M.B. & Zheng, D. (2009) Small RNAs originated from pseudogene: Cis-or tans-acting? PLoS Computer Biology 5: e1000449. https://doi.org/10.1371/journal.pcbi.1000449

  24. He, P., Huang, S., Xiao, G., Zhang, Y. & Yu, J. (2016) Abundant RNA editing sites of chloroplast protein-coding genes in Ginkgo biloba and an evolutionary pattern analysis. BMC Plant Biology 16: 257. https://doi.org/10.1186/s12870-016-0944-8

  25. Hecht, J., Grewe, F. & Knoop, V. (2011) Extreme RNA editing in coding islands and abundant microsatellites in repeat sequences of Selaginella moellendorffii mitochondria: The root of frequent plant mtDNA recombination in early tracheophytes. Genome Biology & Evolution 3: 344–358. https://doi.org/10.1093/gbe/evr027

  26. Hepburn, N.J., Schmidt, D.W. & Mower, J.P. (2012) Loss of two introns from the Magnolia tripetala mitochondrial cox2 gene implicates horizontal gene transfer and gene conversion as a novel mechanism of intron loss. Molecular Biology & Evolution 29: 3111–3120. https://doi.org/10.1093/molbev/mss130

  27. Katoh, K., Kuma, K., Toh, H. & Miyata, T. (2005) MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Research 33: 511–518. https://doi.org/10.1093/nar/gki198

  28. Knie, N., Grewe, F., Fischer, S. & Knoop, V. (2016) Reverse U-to-C editing exceeds C-to-U RNA editing in some ferns–a monilophyte-wide comparison of chloroplast and mitochondrial RNA editing suggests independent evolution of the two processes in both organelles. BMC Evolutionary Biology 16: 134. https://doi.org/10.1186/s12862-016-0707-z

  29. Knoop, V. (2011) When you can’t trust the DNA: RNA editing changes transcript sequences. Cellular & Molecular Life Sciences 68: 567–586. https://doi.org/10.1007/s00018-010-0538-9

  30. Kumar, R.P., Senthilkumar, R., Singh, V. & Mishra, R.K. (2010) Repeat performance: How do genome packaging and regulation depend on simple sequence repeats? Bioessays News & Reviews in Molecular Cellular & Developmental Biology 32: 165–174. https://doi.org/10.1002/bies.200900111

  31. Lanfear, R., Calcott, B., Ho, S.Y.W. & Guindon, S. (2012) Partitionfinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology & Evolution 29: 1695–1701. https://doi.org/10.1093/molbev/mss020

  32. Li, L., Wang, B., Liu, Y. & Qiu, Y.L. (2009) The complete mitochondrial genome sequence of the hornwort Megaceros aenigmaticus shows a mixed mode of conservative yet dynamic evolution in early land plant mitochondrial genomes. Journal of Molecular Evolution 68: 665–678. https://doi.org/10.1007/s00239-009-9240-7

  33. Lilly, J.W. & Havey, M.J. (2001) Small, repetitive DNAs contribute significantly to the expanded mitochondrial genome of cucumber. Genetics 159: 317–328.

  34. Liu, Y., Cox, C.J., Wang, W. & Goffinet, B. (2014a). Mitochondrial phylogenomics of early land plants: mitigating the effects of saturation, compositional heterogeneity and codon usage bias. Systematic Biology 63: 862–878.  https://doi.org/10.1093/sysbio/syu049

  35. Liu, Y., Medina, R. & Goffinet, B. (2014b) 350 my of mitochondrial genome stasis in mosses, an early land plant lineage. Molecular Biology & Evolution 31: 2586–2591. https://doi.org/10.1093/molbev/msu199

  36. Liu, Y., Wang, B., Li, L., Qiu, Y.L. & Xue, J.Y. (2012) Conservative and dynamic evolution of mitochondrial genomes in early land plants. In: Bock, R. & Knoop, V. (Eds.) Genomics of Chloroplasts and Mitochondria. Springer Netherlands, pp. 159–174. https://doi.org/10.1007/978-94-007-2920-9_7

  37. Maddison, W.P. & Maddison, D.R. (2019) Mesquite: a modular system for evolutionary analysis. Version 3.61 [http://www.mesquiteproject.org]

  38. Marechal, A. & Brisson, N. (2010) Recombination and the maintenance of plant organelle genome stability. New Phytologist 186: 299–317. https://doi.org/10.1111/j.1469-8137.2010.03195.x

  39. Villarreal, A J.C., Turmel, M., Bourgouin-Couture, M., Laroche, J., Salazar Allen, N., Li, F.W., Cheng, S., Renzaglia, K. & Lemieux, C. (2018) Genome-wide organellar analyses from the hornwort Leiosporoceros dussii show low frequency of RNA editing. PLoS ONE 13: e0200491. https://doi.org/10.1371/journal.pone.0200491

  40. Morris, J.L., Puttick, M.N., Clark, J.W., Edwards, D., Kenrick, P., Pressel, S., Wellman, C.H., Yang, Z., Schneider, H. & Donoghue, P.C.J. (2018) The timescale of early land plant evolution. Proceedings of the National Academy of Sciences of The United States of America 115: E2274–E2283. https://doi.org/10.1073/pnas.1719588115

  41. Mower, J.P. (2020) Variation in protein gene and intron content among land plant mitogenomes. Mitochondrion 53: 203–213. https://doi.org/10.1016/j.mito.2020.06.002

  42. Mower, J.P., Sloan, D.B. & Alverson, A.J. (2012) Plant mitochondrial genome diversity: The genomics revolution. Heidelberg: Springer Vienna.  https://doi.org/10.1007/978-3-7091-1130-7_9

  43. Myszczynìski, K., Goìrski, P., Sìlipiko, M. & Sawicki, J. (2018) Sequencing of organellar genomes of Gymnomitrion concinnatum (Jungermanniales) revealed the first exception in the structure and gene order of evolutionary stable liverworts mitogenomes. BMC Plant Biology 18: 321. https://doi.org/10.1186/s12870-018-1558-0

  44. Oda, K., Yamato, K., Ohta, E., Nakamura, Y., Takemura, M., Nozato, N., Akashi, K., Kanegae, T., Ogura, Y., Kohchi, T. & Ohyama, K. (1992) Gene organization deduced from the complete sequence of liverwort Marchantia polymorpha mitochondrial DNA: A primitive form of plant mitochondrial genome. Journal of Molecular Biology 223: 1–7. https://doi.org/10.1016/0022-2836(92)90708-R

  45. Oldenkott, B., Yamaguchi, K., Tsuji-Tsukinoki, S., Knie, N. & Knoop V. (2014) Chloroplast RNA editing going extreme: More than 3400 events of C-to-U editing in the chloroplast transcriptome of the lycophyte Selaginella uncinata. RNA-A Publication of The RNA Society 20: 1499–1506. https://doi.org/10.1261/rna.045575.114

  46. One Thousand Plant Transcriptomes Initiative (2019) One thousand plant transcriptomes and the phylogenomics of green plants. Nature 574: 679–685. https://doi.org/10.1038/s41586-019-1693-2

  47. Palmer, J.D. & Herbon, L.A. (1988) Plant mitochondrial DNA evolved rapidly in structure, but slowly in sequence. Journal of Molecular Evolution 28: 87–97. https://doi.org/10.1007/BF02143500

  48. Palmer, J.D., Adams, K.L., Cho, Y., Parkinson, C.L., Qiu, Y.L. & Song, K. (2000) Dynamic evolution of plant mitochondrial genomes: Mobile genes and introns and highly variable mutation rates. Proceedings of the National Academy of Sciences of The United States of America 97: 6960–6966. https://doi.org/10.1073/pnas.97.13.6960

  49. Petersen, G., Cuenca, A., Møller, I.M. & Seberg, O. (2015) Massive gene loss in mistletoe (Viscum, Viscaceae) mitochondria. Scientific Reports 5: 17588. https://doi.org/10.1038/srep17588

  50. Puttick, M.N., Morris, J.L., Williams, T.A., Cox, C.J., Edwards, D., Kenrick, P., Pressel, S., Wellman, C.H., Schneider, H., Pisani, D. & Donoghue, P.C.J. (2018) The interrelationships of land plants and the nature of the ancestral embryophyte. Current Biology 28: 1–13. https://doi.org/10.1016/j.cub.2018.01.063

  51. Quang, M.B., Schmidt, H.A., Olga, C., Dominik, S., Woodhams, M.D., Arndt, V.H. & Lanfear, R. (2020) IQ-TREE2: new models and efficient methods for phylogenetic inference in the genomic era. Molecular Biology & Evolution 37: 1530–1534. https://doi.org/10.1093/molbev/msaa015

  52. Rice, D.W., Alverson, A.J., Richardson, A.O., Young, G.J., Sanchezpuerta, M.V., Munzinger, J., Barry, K., Boore, J.L., Zhang, L., DePamphilis, C.W., Knox, E.B. & Palmer, J.D. (2013) Horizontal transfer of entire genomes via mitochondrial fusion in the angiosperm Amborella. Science 342: 1468–1473. https://doi.org/10.1126/science.1246275

  53. Richardson, A.O., Rice, D.W., Young, G.J., Alverson, A.J. & Palmer, J.D. (2013) The “fossilized” mitochondrial genome of Liriodendron tulipifera: Ancestral gene content and order, ancestral editing sites, and extraordinarily low mutation rate. BMC Biology 11: 29. https://doi.org/10.1186/1741-7007-11-29

  54. Rüdinger, M., Funk, H.T., Rensing, SA, Maier, U.G. & Knoop, V. (2009) RNA editing: only eleven sites are present in the Physcomitrella patens mitochondrial transcriptome and a universal nomenclature proposal. Molecular Genetics & Genomics 281: 473–481. https://doi.org/10.1007/s00438-009-0424-z

  55. Rüdinger, M., Polsakiewicz, M. & Knoop, V. (2008) Organellar RNA editing and plant-specific extensions of pentatricopeptide repeat proteins in jungermanniid but not in marchantiid liverworts. Molecular Biology & Evolution 25: 1405–1414. https://doi.org/10.1093/molbev/msn084

  56. Skippington, E., Barkman, T.J., Rice, D.W. & Palmer, J.D. (2015) Miniaturized mitogenome of the parasitic plant Viscum scurruloideum is extremely divergent and dynamic and has lost all nad genes. Proceedings of the National Academy of Sciences of The United States of America 112: E3515–E3524. https://doi.org/10.1073/pnas.1504491112

  57. Ślipiko, M., Myszczyński, K., Buczkowska-Chmielewska, K., Bączkiewicz, A., Szczecińska, M. & Sawicki, J. (2017) Comparative analysis of four Calypogeia species revealed unexpected change in evolutionarily-stable liverwort mitogenomes. Genes 8: 395. https://doi.org/10.3390/genes8120395

  58. Sloan, D.B. (2013) One ring to rule them all? Genome sequencing provides new insights into the ‘master circle’ model of plant mitochondrial DNA structure. New Phytologist 200: 978–985. https://doi.org/10.1111/nph.12395

  59. Sloan, D.B. (2017) Nuclear and mitochondrial RNA editing systems have opposite effects on protein diversity. Biology Letters 13: 20170314. https://doi.org/10.1098/rsbl.2017.0314

  60. Sloan, D.B., MacQueen, A.H., Alverson, A.J., Palmer, J.D. & Taylor, D.R. (2010) Extensive loss of RNA editing sites in rapidly evolving Silene mitochondrial genomes: Selection vs. Retroprocessing as the driving force. Genetics 185: 1369–1380. https://doi.org/10.1534/genetics.110.118000

  61. Sloan, D.B., Alverson, A.J., Chuckalovcak, J.P., Wu, M., McCauley, D.E., Palmer, J.D. & Taylor, D.R. (2012) Rapid evolution of enormous, multichromosomal genomes in flowering plant mitochondria with exceptionally high mutation rates. PLoS Biology 10: e1001241. https://doi.org/10.1371/journal.pbio.1001241

  62. Sousa, F., Civáň, P., Foster, P.G. & Cox, C.J. (2020) The chloroplast land plant phylogeny: analyses employing better-fitting tree-and site-heterogeneous composition models. Frontiers in Plant Science 11: 1062. https://doi.org/10.3389/fpls.2020.01062

  63. Takenaka, M., Verbitskiy, D., van der Merwe, J.A., Zehrmann, A. & Brennicke, A. (2008) The process of RNA editing in plant mitochondria. Mitochondrion 8: 35–46. https://doi.org/10.1016/j.mito.2007.09.004

  64. Takenaka, M., Zehrmann, A., Verbitskiy, D., Hartel, B. & Brennicke, A. (2013) RNA editing in plants and its evolution. Annual Review of Genetics 47: 335–352. https://doi.org/10.1146/annurev-genet-111212-133519

  65. Talavera, G. & Castresana, J. (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Systematic Biology 56: 564–577. https://doi.org/10.1080/10635150701472164

  66. Vigalondo, B., Yang, L., Draper, I., Lara, F., Garilleti, R., Mazimpaka, V. & Goffinet, B. (2016) Comparing three complete mitochondrial genomes of the moss genus Orthotrichum Hedw. Mitochondrial DNA Part B Resources 1: 179–181. https://doi.org/10.1080/23802359.2016.1149784

  67. Wang, B., Xue, J., Li, L., Yang, L. & Qiu, Y.L. (2009) The complete mitochondrial genome sequence of the liverwort Pleurozia purpurea, reveals extremely conservative mitochondrial genome evolution in liverworts. Current Genetics 55: 601–609. https://doi.org/10.1007/s00294-009-0273-7

  68. Wynn, E.L. & Christensen, A.C. (2019) Repeats of unusual size in plant mitochondrial genomes: Identification, incidence and evolution. Genes, Genomes, Genetics 9: 549–559. https://doi.org/10.1101/376020

  69. Xue, J.Y., Liu, Y., Li, L., Wang, B. & Qiu, Y.L. (2009) The complete mitochondrial genome sequence of the hornwort Phaeoceros laevis: Retention of many ancient pseudogenes and conservative evolution of mitochondrial genomes in hornworts. Current Genetics 56: 53–61. https://doi.org/10.1007/s00294-009-0279-1

  70. Zumkeller, S., Gerke, P. & Knoop, V. (2020) A functional twintron, ‘zombie’ twintrons and a hypermobile group II intron invading itself in plant mitochondria. Nucleic Acids Research 48: 2661–2675. https://doi.org/10.1093/nar/gkz1194