Multiple configurations of the plastid and mitochondrial genomes of Caragana spinosa.
Caragana spinosa
Homologous recombination
Mitochondrial genome
Journal
Planta
ISSN: 1432-2048
Titre abrégé: Planta
Pays: Germany
ID NLM: 1250576
Informations de publication
Date de publication:
13 Oct 2023
13 Oct 2023
Historique:
received:
14
06
2023
accepted:
15
09
2023
medline:
30
10
2023
pubmed:
13
10
2023
entrez:
13
10
2023
Statut:
epublish
Résumé
In this study, we assembled the complete plastome and mitogenome of Caragana spinosa and explored the multiple configurations of the organelle genomes. Caragana spinosa belongs to the Papilionoidea subfamily and has significant pharmaceutical value. To explore the possible interaction between the organelle genomes, we assembled and analyzed the plastome and mitogenome of C. spinosa using the Illumina and Nanopore DNA sequencing data. The plastome of C. spinosa was 129,995 bp belonging to the inverted repeat lacking clade (IRLC), which contained 77 protein-coding genes, 29 tRNA genes, and four rRNA genes. The mitogenome was 378,373 bp long and encoded 54 unique genes, including 33 protein-coding, three ribosomal RNA (rRNA), and 18 transfer RNA (tRNA) genes. In addition to the single circular conformation, alternative conformations mediated by one and four repetitive sequences in the plastome and mitogenome were identified and validated, respectively. The inverted repeat (PDR12, the 12th dispersed repeat sequence in C. spinosa plastome) of plastome mediating recombinant was conserved in the genus Caragana. Furthermore, we identified 14 homologous fragments by comparing the sequences of mitogenome and plastome, including eight complete tRNA genes. A phylogenetic analysis of protein-coding genes extracted from the plastid and mitochondrial genomes revealed congruent topologies. Analyses of sequence divergence found one intergenic region, trnN-GUU-ycf1, exhibiting a high degree of variation, which can be used to develop novel molecular markers to distinguish the nine Caragana species accurately. This plastome and mitogenome of C. spinosa could provide critical information for the molecular breeding of C. spinosa and be used as a reference genome for other species of Caragana. In this study, we assembled the complete plastome and mitogenome of Caragana spinosa and explored the multiple configurations of the organelle genomes.
Identifiants
pubmed: 37831319
doi: 10.1007/s00425-023-04245-6
pii: 10.1007/s00425-023-04245-6
doi:
Substances chimiques
RNA, Transfer
9014-25-9
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
98Subventions
Organisme : CAMS Innovation Fund for Medical Sciences (CIFMS)
ID : 2021-I2M-1-071
Organisme : CAMS Innovation Fund for Medical Sciences (CIFMS)
ID : 2021-1-I2M-022
Organisme : National Natural Science Foundation of China
ID : 81872966
Organisme : National Science and Technology Program during the Twelfth Five-year Plan Period
ID : 2018FY100705
Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Beier S, Thiel T, Münch T, Scholz U, Mascher M (2017) MISA-web: a web server for microsatellite prediction. Bioinformatics (oxford, England) 33(16):2583–2585. https://doi.org/10.1093/bioinformatics/btx198
doi: 10.1093/bioinformatics/btx198
pubmed: 28398459
Benson G (1999) Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 27(2):573–580. https://doi.org/10.1093/nar/27.2.573
doi: 10.1093/nar/27.2.573
pubmed: 9862982
pmcid: 148217
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. https://doi.org/10.3389/fpls.2022.914635
doi: 10.3389/fpls.2022.914635
pubmed: 35783945
pmcid: 9240471
Burki F (2016) Mitochondrial evolution: going, going, gone. Curr Biol 26(10):R410-412. https://doi.org/10.1016/j.cub.2016.04.032
doi: 10.1016/j.cub.2016.04.032
pubmed: 27218846
Carrington M, Roditi I, Williams RO (1987) The structure and transcription of an element interspersed between tandem arrays of mini-exon donor RNA genes in Trypanosoma brucei. Nucleic Acids Res 15(24):10179–10198. https://doi.org/10.1093/nar/15.24.10179
doi: 10.1093/nar/15.24.10179
pubmed: 2827116
pmcid: 339938
Chen Y, Ye W, Zhang Y, Xu Y (2015) High speed BLASTN: an accelerated MegaBLAST search tool. Nucleic Acids Res 43(16):7762–7768. https://doi.org/10.1093/nar/gkv784
doi: 10.1093/nar/gkv784
pubmed: 26250111
pmcid: 4652774
Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, Xia R (2020) TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant 13(8):1194–1202. https://doi.org/10.1016/j.molp.2020.06.009
doi: 10.1016/j.molp.2020.06.009
pubmed: 32585190
Christensen AC (2021) Plant mitochondria are a riddle wrapped in a mystery inside an enigma. J Mol Evol 89(3):151–156. https://doi.org/10.1007/s00239-020-09980-y
doi: 10.1007/s00239-020-09980-y
pubmed: 33486550
Clifton SW, Minx P, Fauron CM, Gibson M, Allen JO, Sun H, Thompson M, Barbazuk WB, Kanuganti S, Tayloe C, Meyer L, Wilson RK, Newton KJ (2004) Sequence and comparative analysis of the maize NB mitochondrial genome. Plant Physiol 136(3):3486–3503. https://doi.org/10.1104/pp.104.044602
doi: 10.1104/pp.104.044602
pubmed: 15542500
pmcid: 527149
Cummings MP, Nugent JM, Olmstead RG, Palmer JD (2003) Phylogenetic analysis reveals five independent transfers of the chloroplast gene rbcL to the mitochondrial genome in angiosperms. Curr Genet 43(2):131–138. https://doi.org/10.1007/s00294-003-0378-3
doi: 10.1007/s00294-003-0378-3
pubmed: 12695853
Dash VB (1994) Materia medica of Tibetan medicine (with illustrations). In: Materia Medica of Tibetan Medicine (with illustrations), pp 694–694
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(1):614. https://doi.org/10.1186/s12864-018-4991-4
doi: 10.1186/s12864-018-4991-4
pubmed: 30107780
pmcid: 6092842
Doyle JJ, Doyle JL, Ballenger JA, Palmer JD (1996) The distribution and phylogenetic significance of a 50-kb chloroplast DNA inversion in the flowering plant family Leguminosae. Mol Phylogenet Evol 5(2):429–438. https://doi.org/10.1006/mpev.1996.0038
doi: 10.1006/mpev.1996.0038
pubmed: 8728401
Drouin G, Daoud H, Xia J (2008) Relative rates of synonymous substitutions in the mitochondrial, chloroplast and nuclear genomes of seed plants. Mol Phylogenet Evol 49(3):827–831. https://doi.org/10.1016/j.ympev.2008.09.009
doi: 10.1016/j.ympev.2008.09.009
pubmed: 18838124
Gu C, Dong B, Xu L, Tembrock LR, Zheng S, Wu Z (2018) The complete chloroplast genome of Heimia myrtifolia and comparative analysis within myrtales. Molecules (Basel, Switzerland). https://doi.org/10.3390/molecules23040846
He W, Chen C, Adedze YMN, Dong X, Xi K, Sun Y, Dang T, Jin D (2020) Multicentric origin and diversification of atp6-orf79-like structures reveal mitochondrial gene flows in Oryza rufipogon and Oryza sativa. Evol Appl 13(9):2284–2299. https://doi.org/10.1111/eva.13022
doi: 10.1111/eva.13022
pubmed: 33005224
pmcid: 7513716
He W, Chen C, Xiang K, Wang J, Zheng P, Tembrock LR, Jin D, Wu Z (2021) The history and diversity of rice domestication as resolved from 1464 complete plastid genomes. Front Plant Sci 12:781793. https://doi.org/10.3389/fpls.2021.781793
doi: 10.3389/fpls.2021.781793
pubmed: 34868182
pmcid: 8637288
Hu JM, Lavin M, Wojciechowski MF, Sanderson MJ (2000) Phylogenetic systematics of the tribe Millettieae (Leguminosae) based on chloroplast trnK/matK sequences and its implications for evolutionary patterns in Papilionoideae. Am J Bot 87(3):418–430. https://doi.org/10.2307/2656638
doi: 10.2307/2656638
pubmed: 10719003
Huang CY, Grünheit N, Ahmadinejad N, Timmis JN, Martin W (2005) Mutational decay and age of chloroplast and mitochondrial genomes transferred recently to angiosperm nuclear chromosomes. Plant Physiol 138(3):1723–1733. https://doi.org/10.1104/pp.105.060327
doi: 10.1104/pp.105.060327
pubmed: 15951485
pmcid: 1176441
Jansen RK, Cai Z, Raubeson LA, Daniell H, Depamphilis CW, Leebens-Mack J, Müller KF, Guisinger-Bellian M, Haberle RC, Hansen AK, Chumley TW, Lee SB, Peery R, McNeal JR, Kuehl JV, Boore JL (2007) Analysis of 81 genes from 64 plastid genomes resolves relationships in angiosperms and identifies genome-scale evolutionary patterns. Proc Natl Acad Sci USA 104(49):19369–19374. https://doi.org/10.1073/pnas.0709121104
doi: 10.1073/pnas.0709121104
pubmed: 18048330
pmcid: 2148296
Jiang M, Chen H, He S, Wang L, Chen AJ, Liu C (2018) Sequencing, characterization, and comparative analyses of the plastome of Caragana rosea var. rosea. Int J Mol Sci. https://doi.org/10.3390/ijms19051419
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(1):241. https://doi.org/10.1186/s13059-020-02154-5
doi: 10.1186/s13059-020-02154-5
pubmed: 32912315
pmcid: 7488116
Kan SL, Shen TT, Ran JH, Wang XQ (2021) Both Conifer II and Gnetales are characterized by a high frequency of ancient mitochondrial gene transfer to the nuclear genome. BMC Biol 19(1):146. https://doi.org/10.1186/s12915-021-01096-z
doi: 10.1186/s12915-021-01096-z
pubmed: 34320951
pmcid: 8317393
Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30(4):772–780. https://doi.org/10.1093/molbev/mst010
doi: 10.1093/molbev/mst010
pubmed: 23329690
pmcid: 3603318
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
doi: 10.1093/bib/bbx108
pubmed: 28968734
Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics (Oxford, England) 23(21):2947–2948. https://doi.org/10.1093/bioinformatics/btm404
Letunic I, Bork P (2021) Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res 49(W1):W293-w296. https://doi.org/10.1093/nar/gkab301
doi: 10.1093/nar/gkab301
pubmed: 33885785
pmcid: 8265157
Lewis SE, Searle SM, Harris N, Gibson M, Lyer V, Richter J, Wiel C, Bayraktaroglu L, Birney E, Crosby MA, Kaminker JS, Matthews BB, Prochnik SE, Smithy CD, Tupy JL, Rubin GM, Misra S, Mungall CJ, Clamp ME (2002) Apollo: a sequence annotation editor. Genome Biol 3(12):Research0082. https://doi.org/10.1186/gb-2002-3-12-research0082
Li H (2018) Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics (oxford, England) 34(18):3094–3100. https://doi.org/10.1093/bioinformatics/bty191
doi: 10.1093/bioinformatics/bty191
pubmed: 29750242
Li HT, Yi TS, Gao LM, Ma PF, Zhang T, Yang JB, Gitzendanner MA, Fritsch PW, Cai J, Luo Y, Wang H, van der Bank M, Zhang SD, Wang QF, Wang J, Zhang ZR, Fu CN, Yang J, Hollingsworth PM, Chase MW, Soltis DE, Soltis PS, Li DZ (2019) Origin of angiosperms and the puzzle of the Jurassic gap. Nat Plants 5(5):461–470. https://doi.org/10.1038/s41477-019-0421-0
doi: 10.1038/s41477-019-0421-0
pubmed: 31061536
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(2):36. https://doi.org/10.1007/s00425-021-03684-3
doi: 10.1007/s00425-021-03684-3
pubmed: 34302538
Lovin DD, Washington KO, deBruyn B, Hemme RR, Mori A, Epstein SR, Harker BW, Streit TG, Severson DW (2009) Genome-based polymorphic microsatellite development and validation in the mosquito Aedes aegypti and application to population genetics in Haiti. BMC Genomics 10:590. https://doi.org/10.1186/1471-2164-10-590
doi: 10.1186/1471-2164-10-590
pubmed: 20003193
pmcid: 3087561
Mackenzie S (1999) Higher plant mitochondria. Plant Cell 11(4):571–586. https://doi.org/10.1105/tpc.11.4.571
doi: 10.1105/tpc.11.4.571
pubmed: 10213779
pmcid: 144202
Mackenzie S, He S, Lyznik A (1994) The elusive plant mitochondrion as a genetic system. Plant Physiol 105(3):775–780. https://doi.org/10.1104/pp.105.3.775
doi: 10.1104/pp.105.3.775
pubmed: 12232241
pmcid: 160723
Magee AM, Aspinall S, Rice DW, Cusack BP, Sémon M, Perry AS, Stefanović S, Milbourne D, Barth S, Palmer JD, Gray JC, Kavanagh TA, Wolfe KH (2010) Localized hypermutation and associated gene losses in legume chloroplast genomes. Genome Res 20(12):1700–1710. https://doi.org/10.1101/gr.111955.110
doi: 10.1101/gr.111955.110
pubmed: 20978141
pmcid: 2989996
Meng Q, Niu Y, Niu X, Roubin RH, Hanrahan JR (2009) Ethnobotany, phytochemistry and pharmacology of the genus Caragana used in traditional Chinese medicine. J Ethnopharmacol 124(3):350–368. https://doi.org/10.1016/j.jep.2009.04.048
doi: 10.1016/j.jep.2009.04.048
pubmed: 19422901
Morgante M, Hanafey M, Powell W (2002) Microsatellites are preferentially associated with nonrepetitive DNA in plant genomes. Nat Genet 30(2):194–200. https://doi.org/10.1038/ng822
doi: 10.1038/ng822
pubmed: 11799393
Mower JP, Sloan DB, Alverson AJ (2012) Plant mitochondrial genome diversity: the genomics revolution. Springer
Naranpanawa DNU, Chandrasekara C, Bandaranayake PCG, Bandaranayake AU (2020) Raw transcriptomics data to gene specific SSRs: a validated free bioinformatics workflow for biologists. Sci Rep 10(1):18236. https://doi.org/10.1038/s41598-020-75270-8
doi: 10.1038/s41598-020-75270-8
pubmed: 33106560
pmcid: 7588437
Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 32(1):268–274. https://doi.org/10.1093/molbev/msu300
doi: 10.1093/molbev/msu300
pubmed: 25371430
Notsu Y, Masood S, Nishikawa T, Kubo N, Akiduki G, Nakazono M, Hirai A, Kadowaki K (2002) The complete sequence of the rice (Oryza sativa L.) mitochondrial genome: frequent DNA sequence acquisition and loss during the evolution of flowering plants. Mol Genet Genomics 268(4):434–445. https://doi.org/10.1007/s00438-002-0767-1
Oldenburg DJ, Bendich AJ (2004) Most chloroplast DNA of maize seedlings in linear molecules with defined ends and branched forms. J Mol Biol 335(4):953–970. https://doi.org/10.1016/j.jmb.2003.11.020
doi: 10.1016/j.jmb.2003.11.020
pubmed: 14698291
Olennikov D, Partilkhaev V (2012) Isolation and densitometric HPTLC analysis of rutin, narcissin, nicotiflorin, and isoquercitrin in Caragana spinosa shoots. J Planar Chromatogr Modern TLC 25(1):30–35. https://doi.org/10.1556/JPC.25.2012.1.5
doi: 10.1556/JPC.25.2012.1.5
Palmer JD, Herbon LA (1988) Plant mitochondrial DNA evolves rapidly in structure, but slowly in sequence. J Mol Evol 28(1–2):87–97. https://doi.org/10.1007/bf02143500
doi: 10.1007/bf02143500
pubmed: 3148746
Park HS, Jayakodi M, Lee SH, Jeon JH, Lee HO, Park JY, Moon BC, Kim CK, Wing RA, Newmaster SG, Kim JY, Yang TJ (2020) Mitochondrial plastid DNA can cause DNA barcoding paradox in plants. Sci Rep 10(1):6112. https://doi.org/10.1038/s41598-020-63233-y
doi: 10.1038/s41598-020-63233-y
pubmed: 32273595
pmcid: 7145815
Putintseva YA, Bondar EI, Simonov EP, Sharov VV, Oreshkova NV, Kuzmin DA, Konstantinov YM, Shmakov VN, Belkov VI, Sadovsky MG, Keech O, Krutovsky KV (2020) Siberian larch (Larix sibirica Ledeb.) mitochondrial genome assembled using both short and long nucleotide sequence reads is currently the largest known mitogenome. BMC Genomics 21(1):654. https://doi.org/10.1186/s12864-020-07061-4
Qu Y, Zhou P, Tong C, Bi C, La Xu (2023) Assembly and analysis of the Populus deltoides mitochondrial genome: the first report of a multicircular mitochondrial conformation for the genus Populus. J Forest Res 34(3):717–733. https://doi.org/10.1007/s11676-022-01511-3
doi: 10.1007/s11676-022-01511-3
Ravi V, Khurana JP, Tyagi AK, Khurana P (2007) An update on chloroplast genomes. Plant Syst Evol 271(1–2):101–122. https://doi.org/10.1007/s00606-007-0608-0
doi: 10.1007/s00606-007-0608-0
Rice P, Longden I, Bleasby A (2000) EMBOSS: the European molecular biology open software suite. Trends in Genetics : TIG 16(6):276–277. https://doi.org/10.1016/s0168-9525(00)02024-2
doi: 10.1016/s0168-9525(00)02024-2
pubmed: 10827456
Richly E, Leister D (2004) NUMTs in sequenced eukaryotic genomes. Mol Biol Evol 21(6):1081–1084. https://doi.org/10.1093/molbev/msh110
doi: 10.1093/molbev/msh110
pubmed: 15014143
Shi L, Chen H, Jiang M, Wang L, Wu X, Huang L, Liu C (2019) CPGAVAS2, an integrated plastome sequence annotator and analyzer. Nucleic Acids Res 47(W1):w65–w73. https://doi.org/10.1093/nar/gkz345
doi: 10.1093/nar/gkz345
pubmed: 31066451
pmcid: 6602467
Shpekina G (1990) Flavonoids of Caragana spinosa. Chem Nat Compd 26(1):95
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 USA 112(27):E3515-3524. https://doi.org/10.1073/pnas.1504491112
doi: 10.1073/pnas.1504491112
pubmed: 26100885
pmcid: 4500244
Skippington E, Barkman TJ, Rice DW, Palmer JD (2017) Comparative mitogenomics indicates respiratory competence in parasitic Viscum despite loss of complex I and extreme sequence divergence, and reveals horizontal gene transfer and remarkable variation in genome size. BMC Plant Biol 17(1):49. https://doi.org/10.1186/s12870-017-0992-8
doi: 10.1186/s12870-017-0992-8
pubmed: 28222679
pmcid: 5319169
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(4):978–985. https://doi.org/10.1111/nph.12395
doi: 10.1111/nph.12395
pubmed: 24712049
Sloan DB, Alverson AJ, Wu M, Palmer JD, Taylor DR (2012) Recent acceleration of plastid sequence and structural evolution coincides with extreme mitochondrial divergence in the angiosperm genus Silene. Genome Biol Evol 4(3):294–306. https://doi.org/10.1093/gbe/evs006
doi: 10.1093/gbe/evs006
pubmed: 22247429
pmcid: 3318436
Sloan DB, Wu Z, Sharbrough J (2018) Correction of persistent errors in Arabidopsis reference mitochondrial genomes. Plant Cell 30(3):525–527. https://doi.org/10.1105/tpc.18.00024
doi: 10.1105/tpc.18.00024
pubmed: 29519893
pmcid: 5894837
Sperisen C, Büchler U, Gugerli F, Mátyás G, Geburek T, Vendramin GG (2001) Tandem repeats in plant mitochondrial genomes: application to the analysis of population differentiation in the conifer Norway spruce. Mol Ecol 10(1):257–263. https://doi.org/10.1046/j.1365-294x.2001.01180.x
doi: 10.1046/j.1365-294x.2001.01180.x
pubmed: 11251804
Sugiyama Y, Watase Y, Nagase M, Makita N, Yagura S, Hirai A, Sugiura M (2005) The complete nucleotide sequence and multipartite organization of the tobacco mitochondrial genome: comparative analysis of mitochondrial genomes in higher plants. Mol Genet Genomics 272(6):603–615. https://doi.org/10.1007/s00438-004-1075-8
doi: 10.1007/s00438-004-1075-8
pubmed: 15583938
Thorvaldsdóttir H, Robinson JT, Mesirov JP (2013) Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform 14(2):178–192. https://doi.org/10.1093/bib/bbs017
doi: 10.1093/bib/bbs017
pubmed: 22517427
Timmis JN, Ayliffe MA, Huang CY, Martin W (2004) Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat Rev Genet 5(2):123–135. https://doi.org/10.1038/nrg1271
doi: 10.1038/nrg1271
pubmed: 14735123
Tsujimura M, Kaneko T, Sakamoto T, Kimura S, Shigyo M, Yamagishi H, Terachi T (2019) Multichromosomal structure of the onion mitochondrial genome and a transcript analysis. Mitochondrion 46:179–186. https://doi.org/10.1016/j.mito.2018.05.001
doi: 10.1016/j.mito.2018.05.001
pubmed: 30006008
Unseld M, Marienfeld JR, Brandt P, Brennicke A (1997) The mitochondrial genome of Arabidopsis thaliana contains 57 genes in 366,924 nucleotides. Nat Genet 15(1):57–61. https://doi.org/10.1038/ng0197-57
doi: 10.1038/ng0197-57
pubmed: 8988169
Wang W, Lanfear R (2019) Long-reads reveal that the chloroplast genome exists in two distinct versions in most plants. Genome Biol Evol 11(12):3372–3381. https://doi.org/10.1093/gbe/evz256
doi: 10.1093/gbe/evz256
pubmed: 31750905
pmcid: 7145664
Wang RJ, Cheng CL, Chang CC, Wu CL, Su TM, Chaw SM (2008) Dynamics and evolution of the inverted repeat-large single copy junctions in the chloroplast genomes of monocots. BMC Evol Biol 8:36. https://doi.org/10.1186/1471-2148-8-36
doi: 10.1186/1471-2148-8-36
pubmed: 18237435
pmcid: 2275221
Wang J, He W, Xiang K, Wu Z, Gu C (2023) Advances in plant phylogeny in the genome era. J Zhejiang A&F Univ 40(1):10. https://doi.org/10.11833/j.issn.2095-0756.20220313
Wick RR, Schultz MB, Zobel J, Holt KE (2015) Bandage: interactive visualization of de novo genome assemblies. Bioinformatics (oxford, England) 31(20):3350–3352. https://doi.org/10.1093/bioinformatics/btv383
doi: 10.1093/bioinformatics/btv383
pubmed: 26099265
Wick RR, Judd LM, Gorrie CL, Holt KE (2017) Unicycler: Resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput Biol 13(6):e1005595. https://doi.org/10.1371/journal.pcbi.1005595
doi: 10.1371/journal.pcbi.1005595
pubmed: 28594827
pmcid: 5481147
Wojciechowski MF, Lavin M, Sanderson MJ (2004) A phylogeny of legumes (Leguminosae) based on analysis of the plastid matK gene resolves many well-supported subclades within the family. Am J Bot 91(11):1846–1862. https://doi.org/10.3732/ajb.91.11.1846
doi: 10.3732/ajb.91.11.1846
pubmed: 21652332
Wolfe KH, Li WH, Sharp PM (1987) Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proc Natl Acad Sci USA 84(24):9054–9058. https://doi.org/10.1073/pnas.84.24.9054
doi: 10.1073/pnas.84.24.9054
pubmed: 3480529
pmcid: 299690
Wu S, Chen J, Li Y, Liu A, Li A, Yin M, Shrestha N, Liu J, Ren G (2021) Extensive genomic rearrangements mediated by repetitive sequences in plastomes of Medicago and its relatives. BMC Plant Biol 21(1):421. https://doi.org/10.1186/s12870-021-03202-3
doi: 10.1186/s12870-021-03202-3
pubmed: 34521343
pmcid: 8438982
Wu ZQ, Liao XZ, Zhang XN, Tembrock LR, Broz A (2022) Genomic architectural variation of plant mitochondria—a review of multichromosomal structuring. J System Evol 60(1):160–168. https://doi.org/10.1111/jse.12655
doi: 10.1111/jse.12655
Wu Z, Waneka G, Sloan DB (2020) The tempo and mode of angiosperm mitochondrial genome divergence inferred from intraspecific variation in Arabidopsis thaliana. G3 (Bethesda, MD) 10(3):1077–1086. https://doi.org/10.1534/g3.119.401023
Wynn EL, Christensen AC (2019) Repeats of unusual size in plant mitochondrial genomes: identification, incidence and evolution. G3 Genesgenet 9(2):549–559. https://doi.org/10.1534/g3.118.200948
Xin H, June L, Yizhi Z, Liqing Z (2006) Interspecific relationships of Caragana microphylla, C. davazamcii and C. korshinskii (Leguminosae) based on ITS and trnL-F data sets. J System 44(2):126–134. https://doi.org/10.1360/aps040077
Yang Z (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24(8):1586–1591. https://doi.org/10.1093/molbev/msm088
doi: 10.1093/molbev/msm088
pubmed: 17483113
Ye J, Coulouris G, Zaretskaya I, Cutcutache I, Rozen S, Madden TL (2012) Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction. BMC Bioinformatics 13:134. https://doi.org/10.1186/1471-2105-13-134
doi: 10.1186/1471-2105-13-134
pubmed: 22708584
pmcid: 3412702
Zhang M, Fritsch PW, Cruz BC (2009) Phylogeny of Caragana (Fabaceae) based on DNA sequence data from rbcL, trnS-trnG, and ITS. Mol Phylogenet Evol 50(3):547–559. https://doi.org/10.1016/j.ympev.2008.12.001
doi: 10.1016/j.ympev.2008.12.001
pubmed: 19100848
Zhang H, Meltzer P, Davis S (2013) RCircos: an R package for Circos 2D track plots. BMC Bioinformatics 14:244. https://doi.org/10.1186/1471-2105-14-244
doi: 10.1186/1471-2105-14-244
pubmed: 23937229
pmcid: 3765848
Zhang D, Gao F, Jakovlić 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(1):348–355. https://doi.org/10.1111/1755-0998.13096
doi: 10.1111/1755-0998.13096
pubmed: 31599058
Zhang M, Fritsch, P.W. (2010) Evolutionary response of Caragana (Fabaceae) to Qinghai–Tibetan Plateau uplift and Asian interior aridification. Plant Syst Evol 288:191–199. https://doi.org/10.1007/s00606-010-0324-z
Zhang M (2004) Ancestral area analysis of the genus Caragara (Leguminosae). Acta Bot Sin 46(3):253–258
Zhou D, Wang A, Li H (1994) Classification and distribntion of sect. Caragana of genus Caragana Fabr.(Fabaceae). J Northeast Normal Univ 2:5