Remarkable mitochondrial genome heterogeneity in Meniocus linifolius (Brassicaceae).
Brassicaceae
Genome recombination
Intracellular transfer
Mitochondria genome (mitogenome)
Structural variation
Journal
Plant cell reports
ISSN: 1432-203X
Titre abrégé: Plant Cell Rep
Pays: Germany
ID NLM: 9880970
Informations de publication
Date de publication:
11 Jan 2024
11 Jan 2024
Historique:
received:
22
08
2023
accepted:
06
11
2023
medline:
11
1
2024
pubmed:
11
1
2024
entrez:
10
1
2024
Statut:
epublish
Résumé
Detailed analyses of 16 genomes identified a remarkable acceleration of mutation rate, hence mitochondrial sequence and structural heterogeneity, in Meniocus linifolius (Brassicaceae). The powerhouse, mitochondria, in plants feature high levels of structural variation, while the encoded genes are normally conserved. However, the substitution rates and spectra of mitochondria DNA within the Brassicaceae, a family with substantial scientific and economic importance, have not been adequately deciphered. Here, by analyzing three newly assembled and 13 known mitochondrial genomes (mitogenomes), we report the highly variable genome structure and mutation rates in Brassicaceae. The genome sizes and GC contents are 196,604 bp and 46.83%, 288,122 bp and 44.79%, and 287,054 bp and 44.93%, for Meniocus linifolius (Mli), Crucihimalaya lasiocarpa (Cla), and Lepidium sativum (Lsa), respectively. In total, 29, 33, and 34 protein-coding genes (PCGs) and 14, 18, and 18 tRNAs are annotated for Mli, Cla, and Lsa, respectively, while all mitogenomes contain one complete circular molecule with three rRNAs and abundant RNA editing sites. The Mli mitogenome features four conformations likely mediated by the two pairs of long repeats, while at the same time seems to have an unusual evolutionary history due to higher GC content, loss of more genes and sequences, but having more repeats and plastid DNA insertions. Corroborating with these, an ambiguous phylogenetic position with long branch length and elevated synonymous substitution rate in nearly all PCGs are observed for Mli. Taken together, our results reveal a high level of mitogenome heterogeneity at the family level and provide valuable resources for further understanding the evolutionary pattern of organelle genomes in Brassicaceae.
Identifiants
pubmed: 38200362
doi: 10.1007/s00299-023-03102-w
pii: 10.1007/s00299-023-03102-w
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
36Subventions
Organisme : Strategic Priority Research Program (Type-B), Chinese Academy of Science
ID : XDB31000000
Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Adams KL, Qiu YL, Stoutemyer M, Palmer JD (2002) Punctuated evolution of mitochondrial gene content: high and variable rates of mitochondrial gene loss and transfer to the nucleus during angiosperm evolution. Proc Natl Acad Sci U S A 99:9905–9912
pubmed: 12119382
pmcid: 126597
doi: 10.1073/pnas.042694899
Androsiuk P, Paukszto L, Jastrzebski JP, Milarska SE, Okorski A, Pszczolkowska A (2022) Molecular Diversity and Phylogeny Reconstruction of Genus Colobanthus (Caryophyllaceae) Based on Mitochondrial Gene Sequences. Genes (basel) 13:1060
pubmed: 35741822
doi: 10.3390/genes13061060
Beier S, Thiel T, Munch T, Scholz U, Mascher M (2017) MISA-web: a web server for microsatellite prediction. Bioinformatics 33:2583–2585
pubmed: 28398459
pmcid: 5870701
doi: 10.1093/bioinformatics/btx198
Beilstein MA, Al-Shehbaz IA, Kellogg EA (2006) Brassicaceae phylogeny and trichome evolution. Am J Bot 93:607–619
pubmed: 21646222
doi: 10.3732/ajb.93.4.607
Benson G (1999) Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 27:573–580
pubmed: 9862982
pmcid: 148217
doi: 10.1093/nar/27.2.573
Bergthorsson U, Adams KL, Thomason B, Palmer JD (2003) Widespread horizontal transfer of mitochondrial genes in flowering plants. Nature 424:197–201
pubmed: 12853958
doi: 10.1038/nature01743
Bi C, Qu Y, Hou J, Wu K, Ye N, Yin T (2022) Deciphering the Multi-Chromosomal Mitochondrial Genome of Populus simonii. Front Plant Sci 13:914635
pubmed: 35783945
pmcid: 9240471
doi: 10.3389/fpls.2022.914635
Chateigner-Boutin AL, Small I (2010) Plant RNA editing. RNA Biol 7:213–219
pubmed: 20473038
doi: 10.4161/rna.7.2.11343
Chaw SM, Shih AC, Wang D, Wu YW, Liu SM, Chou TY (2008) The mitochondrial genome of the gymnosperm Cycas taitungensis contains a novel family of short interspersed elements, Bpu sequences, and abundant RNA editing sites. Mol Biol Evol 25:603–615
pubmed: 18192697
doi: 10.1093/molbev/msn009
Chen Y, Ye W, Zhang Y, Xu Y (2015) High speed BLASTN: an accelerated MegaBLAST search tool. Nucleic Acids Res 43:7762–7768
pubmed: 26250111
pmcid: 4652774
doi: 10.1093/nar/gkv784
Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, Xia R (2020a) TBtools: An Integrative Toolkit Developed for Interactive Analyses of Big Biological Data. Mol Plant 13:1194–1202
pubmed: 32585190
doi: 10.1016/j.molp.2020.06.009
Chen H, German DA, Al-Shehbaz IA, Yue J, Sun H (2020b) Phylogeny of Euclidieae (Brassicaceae) based on plastome and nuclear ribosomal DNA data. Mol Phylogenet Evol 153:106940
pubmed: 32818597
doi: 10.1016/j.ympev.2020.106940
Cheng Y, He X, Priyadarshani S, Wang Y, Ye L, Shi C, Ye K, Zhou Q, Luo Z, Deng F, Cao L, Zheng P, Aslam M, Qin Y (2021) Assembly and comparative analysis of the complete mitochondrial genome of Suaeda glauca. BMC Genomics 22:167
pubmed: 33750312
pmcid: 7941912
doi: 10.1186/s12864-021-07490-9
Cho Y, Mower JP, Qiu YL, Palmer JD (2004) Mitochondrial substitution rates are extraordinarily elevated and variable in a genus of flowering plants. Proc Natl Acad Sci U S A 101:17741–17746
pubmed: 15598738
pmcid: 539783
doi: 10.1073/pnas.0408302101
Danecek P, Bonfield JK, Liddle J, Marshall J, Ohan V, Pollard MO, Whitwham A, Keane T, McCarthy SA, Davies RM, Li H (2021) Twelve years of SAMtools and BCFtools. Gigascience 10:giab008
pubmed: 33590861
pmcid: 7931819
doi: 10.1093/gigascience/giab008
Dong S, Zhao C, Chen F, Liu Y, Zhang S, Wu H, Zhang L, Liu Y (2018) The complete mitochondrial genome of the early flowering plant Nymphaea colorata is highly repetitive with low recombination. BMC Genomics 19:614
pubmed: 30107780
pmcid: 6092842
doi: 10.1186/s12864-018-4991-4
Edera AA, Small I, Milone DH, Sanchez-Puerta MV (2021) Deepred-Mt: Deep representation learning for predicting C-to-U RNA editing in plant mitochondria. Comput Biol Med 136:104682
pubmed: 34343887
doi: 10.1016/j.compbiomed.2021.104682
Fan W, Liu F, Jia Q, Du H, Chen W, Ruan J, Lei J, Li DZ, Mower JP, Zhu A (2022) Fragaria mitogenomes evolve rapidly in structure but slowly in sequence and incur frequent multinucleotide mutations mediated by microinversions. New Phytol 236:745–759
pubmed: 35731093
doi: 10.1111/nph.18334
Feng L, Lin H, Kang M, Ren Y, Yu X, Xu Z, Wang S, Li T, Yang W, Hu Q (2022) A chromosome-level genome assembly of an alpine plant Crucihimalaya lasiocarpa provides insights into high-altitude adaptation. DNA Res 29:dsac0044
doi: 10.1093/dnares/dsac004
Franzke A, German D, Al-Shehbaz IA, Mummenhoff K (2009) Arabidopsis family ties: molecular phylogeny and age estimates in Brassicaceae. Taxon 58:425–437
doi: 10.1002/tax.582009
Galtier N (2011) The intriguing evolutionary dynamics of plant mitochondrial DNA. BMC Biol 9:61
pubmed: 21951676
pmcid: 3181201
doi: 10.1186/1741-7007-9-61
German DA, Hendriks KP, Koch MA, Lens F, Lysak MA, Bailey CD, Mummenhoff K, Al-Shehbaz IA (2023) An updated classification of the Brassicaceae (Cruciferae). PhytoKeys 220:127–144
pubmed: 37251613
pmcid: 10209616
doi: 10.3897/phytokeys.220.97724
Grewe F, Viehoever P, Weisshaar B, Knoop V (2009) A trans-splicing group I intron and tRNA-hyperediting in the mitochondrial genome of the lycophyte Isoetes engelmannii. Nucleic Acids Res 37:5093–5104
pubmed: 19553190
pmcid: 2731911
doi: 10.1093/nar/gkp532
Grewe F, Edger PP, Keren I, Sultan L, Pires JC, Ostersetzer-Biran O, Mower JP (2014) Comparative analysis of 11 Brassicales mitochondrial genomes and the mitochondrial transcriptome of Brassica oleracea. Mitochondrion 19(Pt B):135–143
pubmed: 24907441
doi: 10.1016/j.mito.2014.05.008
Gualberto JM, Mileshina D, Wallet C, Niazi AK, Weber-Lotfi F, Dietrich A (2014) The plant mitochondrial genome: dynamics and maintenance. Biochimie 100:107–120
pubmed: 24075874
doi: 10.1016/j.biochi.2013.09.016
Guo X, Liu J, Hao G, Zhang L, Mao K, Wang X, Zhang D, Ma T, Hu Q, Al-Shehbaz IA, Koch MA (2017) Plastome phylogeny and early diversification of Brassicaceae. BMC Genomics 18:176
pubmed: 28209119
pmcid: 5312533
doi: 10.1186/s12864-017-3555-3
Gupta RS, Golding GB (1996) The origin of the eukaryotic cell. Trends Biochem Sci 21:166–171
pubmed: 8871398
doi: 10.1016/S0968-0004(96)20013-1
He W, Yang J, Jing Y, Xu L, Yu K, Fang X (2023) NGenomeSyn: an easy-to-use and flexible tool for publication-ready visualization of syntenic relationships across multiple genomes. Bioinformatics 39:btad121
pubmed: 36883694
pmcid: 10027429
doi: 10.1093/bioinformatics/btad121
Hendriks KP, Kiefer C, Al-Shehbaz IA, Bailey CD, Hooft van Huysduynen A, Nikolov LA, Nauheimer L, Zuntini AR, German DA, Franzke A, Koch MA, Lysak MA, Toro-Nunez O, Ozudogru B, Invernon VR, Walden N, Maurin O, Hay NM, Shushkov P, Mandakova T, Schranz ME, Thulin M, Windham MD, Resetnik I, Spaniel S, Ly E, Pires JC, Harkess A, Neuffer B, Vogt R, Brauchler C, Rainer H, Janssens SB, Schmull M, Forrest A, Guggisberg A, Zmarzty S, Lepschi BJ, Scarlett N, Stauffer FW, Schonberger I, Heenan P, Baker WJ, Forest F, Mummenhoff K, Lens F (2023) Global Brassicaceae phylogeny based on filtering of 1,000-gene dataset. Curr Biol 33:e4056
Hohmann N, Wolf EM, Lysak MA, Koch MA (2015) A Time-Calibrated Road Map of Brassicaceae Species Radiation and Evolutionary History. Plant Cell 27:2770–2784
pubmed: 26410304
pmcid: 4682323
Huang C H, Sun R, Hu Y, Zeng LP, Zhang N, Cai LM, Zhang Q, Koch MA, Al-Shehbaz IA, Edger PP, Pires JC, Tan DY, Zhong Y, Ma H (2016) Resolution of brassicaceae phylogeny using nuclear genes uncovers nested radiations and supports convergent morphological evolution. Mol Biol Evol 33:394–412
pubmed: 26516094
doi: 10.1093/molbev/msv226
Jin JJ, Yu WB, Yang JB, Song Y, dePamphilis CW, Yi TS, Li DZ (2020) GetOrganelle: a fast and versatile toolkit for accurate de novo assembly of organelle genomes. Genome Biol 21:241
pubmed: 32912315
pmcid: 7488116
doi: 10.1186/s13059-020-02154-5
Kim D, Paggi JM, Park C, Bennett C, Salzberg SL (2019) Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. Nat Biotechnol 37:907–915
pubmed: 31375807
pmcid: 7605509
doi: 10.1038/s41587-019-0201-4
Kitazaki K, Kubo T (2010) Cost of Having the Largest Mitochondrial Genome: Evolutionary Mechanism of Plant Mitochondrial Genome. J Bot 2010:1–12
doi: 10.1155/2010/620137
Klingenberg M (2008) The ADP and ATP transport in mitochondria and its carrier. Biochim Biophys Acta 1778:1978–2021
pubmed: 18510943
doi: 10.1016/j.bbamem.2008.04.011
Kolmogorov M, Yuan J, Lin Y, Pevzner PA (2019) Assembly of long, error-prone reads using repeat graphs. Nat Biotechnol 37:540–546
pubmed: 30936562
doi: 10.1038/s41587-019-0072-8
Kozik A, Rowan BA, Lavelle D, Berke L, Schranz ME, Michelmore RW, Christensen AC (2019) The alternative reality of plant mitochondrial DNA: One ring does not rule them all. PLoS Genet 15:e1008373
pubmed: 31469821
pmcid: 6742443
doi: 10.1371/journal.pgen.1008373
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 29:4633–4642
pubmed: 11713313
pmcid: 92531
doi: 10.1093/nar/29.22.4633
Lai C, Wang J, Kan S, Zhang S, Li P, Reeve WG, Wu Z, Zhang Y (2022) Comparative analysis of mitochondrial genomes of Broussonetia spp. (Moraceae) reveals heterogeneity in structure, synteny, intercellular gene transfer, and RNA editing. Front Plant Sci 13:1052151
pubmed: 36531410
pmcid: 9751378
doi: 10.3389/fpls.2022.1052151
Lee E, Harris N, Gibson M, Chetty R, Lewis S (2009) Apollo: a community resource for genome annotation editing. Bioinformatics 25:1836–1837
pubmed: 19439563
doi: 10.1093/bioinformatics/btp314
Li H (2021) New strategies to improve minimap2 alignment accuracy. Bioinformatics 37:4572–4574
pubmed: 34623391
pmcid: 8652018
doi: 10.1093/bioinformatics/btab705
Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754–1760
pubmed: 19451168
pmcid: 2705234
doi: 10.1093/bioinformatics/btp324
Li J, Ye C (2020) Genome-wide analysis of microsatellite and sex-linked marker identification in Gleditsia sinensis. BMC Plant Biol 20:338
pubmed: 32680463
pmcid: 7367340
doi: 10.1186/s12870-020-02551-9
Li J, Xu Y, Shan Y, Pei X, Yong S, Liu C, Yu J (2021) Assembly of the complete mitochondrial genome of an endemic plant, Scutellaria tsinyunensis, revealed the existence of two conformations generated by a repeat-mediated recombination. Planta 254:36
pubmed: 34302538
doi: 10.1007/s00425-021-03684-3
Liberatore KL, Dukowic-Schulze S, Miller ME, Chen C, Kianian SF (2016) The role of mitochondria in plant development and stress tolerance. Free Radic Biol Med 100:238–256
pubmed: 27036362
doi: 10.1016/j.freeradbiomed.2016.03.033
Lin Q, Braukmann TWA, Soto Gomez M, Mayer JLS, Pinheiro F, Merckx V, Stefanovic S, Graham SW (2022) Mitochondrial genomic data are effective at placing mycoheterotrophic lineages in plant phylogeny. New Phytol 236:1908–1921
pubmed: 35731179
doi: 10.1111/nph.18335
Liu F, Fan W, Yang JB, Xiang CL, Mower JP, Li DZ, Zhu A (2020a) Episodic and guanine-cytosine-biased bursts of intragenomic and interspecific synonymous divergence in Ajugoideae (Lamiaceae) mitogenomes. New Phytol 228:1107–1114
pubmed: 32558926
doi: 10.1111/nph.16753
Liu LM, Du XY, Guo C, Li DZ (2020b) Resolving robust phylogenetic relationships of core Brassicaceae using genome skimming data. J Syst Evol 59:442–453
doi: 10.1111/jse.12666
Liu J, Ni Y, Liu C (2023a) Polymeric structure of the Cannabis sativa L. mitochondrial genome identified with an assembly graph model. Gene 853:147081
pubmed: 36470482
doi: 10.1016/j.gene.2022.147081
Liu Q, Yuan H, Xu J, Cui D, Xiong G, Schwarzacher T, Heslop-Harrison JS (2023b) The mitochondrial genome of the diploid oat Avena longiglumis. BMC Plant Biol 23:218
pubmed: 37098475
pmcid: 10131481
doi: 10.1186/s12870-023-04217-8
Lukes J, Kaur B, Speijer D (2021) RNA Editing in Mitochondria and Plastids: Weird and Widespread. Trends Genet 37:99–102
pubmed: 33203574
doi: 10.1016/j.tig.2020.10.004
Mackenzie S, McIntosh L (1999) Higher plant mitochondria. Plant Cell 11:571–586
pubmed: 10213779
pmcid: 144202
doi: 10.1105/tpc.11.4.571
Mower JP, Sloan DB, Alverson AJ (2012) Plant Mitochondrial Genome Diversity: The Genomics Revolution. In: Wendel JF, Greilhuber J, Dolezel J, Leitch IJ (eds) Plant Genome Diversity, vol 1. Springer Vienna, Vienna, pp 123–144
doi: 10.1007/978-3-7091-1130-7_9
Ng S, De Clercq I, Van Aken O, Law SR, Ivanova A, Willems P, Giraud E, Van Breusegem F, Whelan J (2014) Anterograde and retrograde regulation of nuclear genes encoding mitochondrial proteins during growth, development, and stress. Mol Plant 7:1075–1093
pubmed: 24711293
doi: 10.1093/mp/ssu037
Nikolov LA, Shushkov P, Nevado B, Gan X, Al-Shehbaz IA, Filatov D, Bailey CD, Tsiantis M (2019) Resolving the backbone of the Brassicaceae phylogeny for investigating trait diversity. New Phytol 222:1638–1651
pubmed: 30735246
doi: 10.1111/nph.15732
Palmer JD, Herbon LA (1988) Plant mitochondrial DNA evolves rapidly in structure, but slowly in sequence. J Mol Evol 28:87–97
pubmed: 3148746
doi: 10.1007/BF02143500
Patat AS, Sen F, Erdogdu BS, Uncu AT, Uncu AO (2022) Construction and characterization of a de novo draft genome of garden cress (Lepidium sativum L.). Funct Integr Genomics 22:879–889
pubmed: 35596045
doi: 10.1007/s10142-022-00866-4
Petersen G, Anderson B, Braun HP, Meyer EH, Moller IM (2020) Mitochondria in parasitic plants. Mitochondrion 52:173–182
pubmed: 32224234
doi: 10.1016/j.mito.2020.03.008
Pond SL, Frost SD, Muse SV (2005) HyPhy: hypothesis testing using phylogenies. Bioinformatics 21:676–679
pubmed: 15509596
doi: 10.1093/bioinformatics/bti079
Qu XJ, Moore MJ, Li DZ, Yi TS (2019) PGA: a software package for rapid, accurate, and flexible batch annotation of plastomes. Plant Methods 15:50
pubmed: 31139240
pmcid: 6528300
doi: 10.1186/s13007-019-0435-7
Qu Y, Zhou P, Tong C, Bi C, La Xu (2022) Assembly and analysis of the Populus deltoides mitochondrial genome: the first report of a multicircular mitochondrial conformation for the genus Populus. Journal of Forestry Research 34:717–733
doi: 10.1007/s11676-022-01511-3
Richardson AO, Rice DW, Young GJ, Alverson AJ, Palmer JD (2013) The “fossilized” mitochondrial genome of Liriodendron tulipifera: ancestral gene content and order, ancestral editing sites, and extraordinarily low mutation rate. BMC Biol 11:29
pubmed: 23587068
pmcid: 3646698
doi: 10.1186/1741-7007-11-29
Robinson JT, Thorvaldsdottir H, Turner D, Mesirov JP (2023) igv.js: an embeddable JavaScript implementation of the Integrative Genomics Viewer (IGV). Bioinformatics 39:btac830
pubmed: 36562559
doi: 10.1093/bioinformatics/btac830
Shen W, Le S, Li Y, Hu F (2016) SeqKit: A Cross-Platform and Ultrafast Toolkit for FASTA/Q File Manipulation. PLoS ONE 11:e0163962
pubmed: 27706213
pmcid: 5051824
doi: 10.1371/journal.pone.0163962
Skippington E, Barkman TJ, Rice DW, Palmer JD (2015) Miniaturized mitogenome of the parasitic plant Viscum scurruloideum is extremely divergent and dynamic and has lost all nad genes. Proc Natl Acad Sci U S A 112:E3515-3524
pubmed: 26100885
pmcid: 4500244
doi: 10.1073/pnas.1504491112
Sloan DB (2013) One ring to rule them all? Genome sequencing provides new insights into the ‘master circle’ model of plant mitochondrial DNA structure. New Phytol 200:978–985
pubmed: 24712049
doi: 10.1111/nph.12395
Sloan DB, Alverson AJ, Chuckalovcak JP, Wu M, McCauley DE, Palmer JD, Taylor DR (2012) Rapid evolution of enormous, multichromosomal genomes in flowering plant mitochondria with exceptionally high mutation rates. PLoS Biol 10:e1001241
pubmed: 22272183
pmcid: 3260318
doi: 10.1371/journal.pbio.1001241
Timmis JN, Ayliffe MA, Huang CY, Martin W (2004) Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat Rev Genet 5:123–135
pubmed: 14735123
doi: 10.1038/nrg1271
Walden N, German DA, Wolf EM, Kiefer M, Rigault P, Huang XC, Kiefer C, Schmickl R, Franzke A, Neuffer B, Mummenhoff K, Koch MA (2020) Nested whole-genome duplications coincide with diversification and high morphological disparity in Brassicaceae. Nat Commun 11:3795
pubmed: 32732942
pmcid: 7393125
doi: 10.1038/s41467-020-17605-7
Wick RR, Schultz MB, Zobel J, Holt KE (2015) Bandage: interactive visualization of de novo genome assemblies. Bioinformatics 31:3350–3352
pubmed: 26099265
pmcid: 4595904
doi: 10.1093/bioinformatics/btv383
Wick RR, Judd LM, Gorrie CL, Holt KE (2017) Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLOS Comput Biol 13: e1005595
pubmed: 28594827
pmcid: 5481147
doi: 10.1371/journal.pcbi.1005595
Wolfe KH, Li WH, Sharp PM (1987) Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proc Natl Acad Sci U S A 84:9054–9058
pubmed: 3480529
pmcid: 299690
doi: 10.1073/pnas.84.24.9054
Wynn EL, Christensen AC (2019) Repeats of Unusual Size in Plant Mitochondrial Genomes: Identification, Incidence and Evolution. G3 (bethesda) 9:549–559
pubmed: 30563833
doi: 10.1534/g3.118.200948
Xia C, Li J, Zuo Y, He P, Zhang H, Zhang X, Wang B, Zhang J, Yu J, Deng H (2023) Complete mitochondrial genome of Thuja sutchuenensis and its implications on evolutionary analysis of complex mitogenome architecture in Cupressaceae. BMC Plant Biol 23:84
pubmed: 36750935
pmcid: 9903464
doi: 10.1186/s12870-023-04054-9
Xu S, Teng K, Zhang H, Wu J, Duan L, Zhang H, Wen H, Teng W, Yue Y, Fan X (2023) The first complete mitochondrial genome of Carex (C. breviculmis): a significantly expanded genome with highly structural variations. Planta 258:43
pubmed: 37450262
doi: 10.1007/s00425-023-04169-1
Yang H, Li W, Yu X, Zhang X, Zhang Z, Liu Y, Wang W, Tian X (2021) Insights into molecular structure, genome evolution and phylogenetic implication through mitochondrial genome sequence of Gleditsia sinensis. Sci Rep 11:14850
pubmed: 34290263
pmcid: 8295344
doi: 10.1038/s41598-021-93480-6
Yang JX, Dierckxsens N, Bai MZ, Guo YY (2023) Multichromosomal Mitochondrial Genome of Paphiopedilum micranthum: Compact and Fragmented Genome, and Rampant Intracellular Gene Transfer. Int J Mol Sci 24:3976
pubmed: 36835385
pmcid: 9966765
doi: 10.3390/ijms24043976
Zhang D, Gao F, Jakovlic I, Zou H, Zhang J, Li WX, Wang GT (2020) PhyloSuite: An integrated and scalable desktop platform for streamlined molecular sequence data management and evolutionary phylogenetics studies. Mol Ecol Resour 20:348–355
pubmed: 31599058
doi: 10.1111/1755-0998.13096
Zhang X, Shan Y, Li J, Qin Q, Yu J, Deng H (2023) Assembly of the Complete Mitochondrial Genome of Pereskia aculeata Revealed That Two Pairs of Repetitive Elements Mediated the Recombination of the Genome. Int J Mol Sci 24:8366
pubmed: 37176072
pmcid: 10179450
doi: 10.3390/ijms24098366
Zhou W, Armijos CE, Lee C, Lu R, Wang J, Ruhlman TA, Jansen RK, Jones AM, Jones CD (2023) Plastid Genome Assembly Using Long-read data. Mol Ecol Resour 23:1442–1457
pubmed: 36939021
pmcid: 10354735
doi: 10.1111/1755-0998.13787
Zhu A, Guo W, Jain K, Mower JP (2014) Unprecedented heterogeneity in the synonymous substitution rate within a plant genome. Mol Biol Evol 31:1228–1236
pubmed: 24557444
doi: 10.1093/molbev/msu079