Abstract
Silene latifolia is an herbaceous plant with great invasive potential. Spread along trade routes from Europe to almost all continents, white campion became particularly widespread in North America. We sequenced the chloroplast genome of S. latifolia subsp. alba from a native range in southeast Fennoscandia. The chloroplast genome of native S. latifolia subsp. alba forms a 151,747-bp circle, has two inverted repeat regions (25,993 bp each), large single copy (82,708 bp), and small single copy (17,106 bp) regions. It contains 77 protein-coding genes, 30 tRNA genes, and four rRNA genes. SSRs and long DNA repeats were identified. Comparison of a newly sequenced plastome of S. latifolia subsp. alba with plastomes of invasive specimens of species from North America and Japan revealed a high level of single nucleotide polymorphisms (SNPs) among them. A total of 214 SNPs were found, among which 110 were identified in intergenic spacers, 74 in exons, and 30 in introns. Intraspecific shifts in inverted repeat boundaries were identified. Our research suggests that high polymorphic regions may be potential molecular markers for population studies and that high intraspecific genetic polymorphism may contribute to a species’ invasive success.
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The newly generated sequence was uploaded in NCBI GenBank, accession number MN244687.
References
Baker HG (1948) Stages in invasion and replacement demonstrated by species of Melandrium. J Ecol 36:96. https://doi.org/10.2307/2256649
Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477. https://doi.org/10.1089/cmb.2012.0021
Bernasconi G, Antonovics J, Biere A, Charlesworth D, Delph LF, Filatov D, Giraud T, Hood ME, Marais GAB, McCauley D, Pannell JR, Shykoff JA, Vyskot B, Wolfe LM, Widmer A (2009) Silene as a model system in ecology and evolution. Heredity (Edinb) 103:5–14. https://doi.org/10.1038/hdy.2009.34
Blair AC, Wolfe LM (2004) The evolution of an invasive plant: an experimental study with Silene latifolia. Ecology 85:3035–3042. https://doi.org/10.1890/04-0341
Bosi E, Donati B, Galardini M, Brunetti S, Sagot MF, Lió P, Crescenzi P, Fani R, Fondi M (2015) MeDuSa: a multi-draft based scaffolder. Bioinformatics 31:2443–2451. https://doi.org/10.1093/bioinformatics/btv171
Brudno M, Malde S, Poliakov A, Do CB, Couronne O, Dubchak I, Batzoglou S (2003) Glocal alignment: finding rearrangements during alignment. Bioinformatics 19:i54–i62. https://doi.org/10.1093/bioinformatics/btg1005
Bushnell B (n.d.) BBMap: a fast, accurate, Splice-Aware Aligner https://jgi.doe.gov/data-and-tools/bbtools/. Accessed 22 Oct 2019
Castillo DM, Kula AAR, Dötterl S, Dudash MR, Fenster CB (2014) Invasive Silene latifolia may benefit from a native pollinating seed predator, Hadena ectypa, in North America. Int J Plant Sci 175:80–91. https://doi.org/10.1086/673536
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
Chater AO, Walters SM (1964) Silene L. In: Tutin TG, Heywood VH, Burges NA et al (eds) Flora Europeae Volume 1 Lycopodiaceae to Plantanaceae. Cambridge University Press, Cambridge, pp 158–181
Darriba D, Taboada GL, Doallo R, Posada D (2012) JModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772
Erixon P, Oxelman B (2008) Whole-gene positive selection, elevated synonymous substitution rates, duplication, and indel evolution of the chloroplast clpP1 gene. PLoS One 3:e1386. https://doi.org/10.1371/journal.pone.0001386
Frazer KA, Pachter L, Poliakov A, Rubin EM, Dubchak I (2004) VISTA: computational tools for comparative genomics. Nucleic Acids Res 32:W273–W279. https://doi.org/10.1093/nar/gkh458
Greiner S, Lehwark P, Bock R (2019) OrganellarGenomeDRAW (OGDRAW) version 1.3.1: expanded toolkit for the graphical visualization of organellar genomes. Nucleic Acids Res 47:W59–W64. https://doi.org/10.1093/nar/gkz238
Gualberto JM, Handa H, Grienenberger JM (1995) Isolation and fractionation of plant mitochondria and chloroplasts: specific examples. Methods Cell Biol 50:161–175
Gurusamy R, Lee DH, Park SJ (2016) The complete chloroplast genome sequence of Dianthus superbus var. longicalycinus. Mitochondrial DNA part a, DNA mapping. Seq Anal 27:2015–2017. https://doi.org/10.3109/19401736.2014.974167
Invasive Plant Atlas of the United States (n.d.) https://www.invasiveplantatlas.org/. Accessed 22 Oct 2019
Invasive Species Compendium (n.d.) https://www.cabi.org/isc. Accessed 22 Oct 2019
Jenkins C, Keller SR (2011) A phylogenetic comparative study of preadaptation for invasiveness in the genus Silene (Caryophyllaceae). Biol Invasions 13:1471–1486. https://doi.org/10.1007/s10530-010-9907-4
Kang J-S, Lee Y, Kwak M (2017) The complete chloroplast genome sequences of Lychnis wilfordii and Silene capitata and comparative analyses with other Caryophyllaceae genomes. https://doi.org/10.1371/journal.pone.0172924
Kassambara A (2020) Ggpubr: “ggplot2” based publication ready plots R package version 0.2.5. https://CRAN.R-project.org/package=ggpubr. Accessed 8 Mai 2020
Katoh K, Standley DM (2013) Article fast track MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780. https://doi.org/10.1093/molbev/mst010
Kazama Y, Sugiyanna R, Matsunaga S, Shibata F, Uchida W, Hizume M, Kawano S (2003) Organization of the KpnI family of chromosomal distal-end satellite DNAs in Silene latifolia. J Plant Res 116:317–326
Keller SR, Gilbert KJ, Fields PD, Taylor DR (2012) Bayesian inference of a complex invasion history revealed by nuclear and chloroplast genetic diversity in the colonizing plant, Silene latifolia. Mol Ecol 21:4721–4734. https://doi.org/10.1111/j.1365-294X.2012.05751.x
Kim K, Lee SC, Lee J, Lee HO, Joh HJ, Kim NH, Park HS, Yang TJ (2015) Comprehensive survey of genetic diversity in chloroplast genomes and 45S nrDNAs within Panax ginseng species. PLoS One 10:e0117159. https://doi.org/10.1371/journal.pone.0117159
Kim Y, Heo KI, Park J (2019) The second complete chloroplast genome sequence of Pseudostellaria palibiniana (Takeda) Ohwi (Caryophyllaceae): intraspecies variations based on geographical distribution. Mitochondrial DNA Part B Resour 4:1310–1311. https://doi.org/10.1080/23802359.2019.1591179
Korber B (2000) HIV signature and sequence variation analysis. In: Rodrigo AG, Learn GH (eds) Computational analysis of HIV molecular sequences. Kluwer Academic Publishers, Dordrecht, pp 55–72
Krüger M, Abeyawardana OAJ, Juříček M, Krüger C, Štorchová H (2019) Variation in plastid genomes in the gynodioecious species Silene vulgaris. BMC Plant Biol 19:1–15. https://doi.org/10.1186/s12870-019-2193-0
Kryazhimskiy S, Plotkin JB (2008) The population genetics of dN/dS. PLoS Genet 4:e1000304. https://doi.org/10.1371/journal.pgen.1000304
Kulikov VS (1995) Where is the southern boundary of Fennoscandia? Bull Geol Soc Finl 67:73–75
Langmead B, Salzberg SL (2012) Fast gapped-read alignment with bowtie 2. Nat Methods 9:357–359. https://doi.org/10.1038/nmeth.1923
Lee HO, Joh HJ, Kim K, Lee SC, Kim NH, Park JY, Park HS, Park MS, Kim S, Kwak M, Kim KY, Lee WK, Yang TJ (2019) Dynamic chloroplast genome rearrangement and DNA barcoding for three Apiaceae species known as the medicinal herb “bang-poong.”. Int J Mol Sci 20:2196. https://doi.org/10.3390/ijms20092196
Lehwark P, Greiner S (2019) GB2sequin - a file converter preparing custom GenBank files for database submission. Genomics 111:759–761. https://doi.org/10.1016/j.ygeno.2018.05.003
Lihua Z, Zhengyi W, Liden M, Oxelman B (2001) SILENE L. In: Flora of China vol. 6 (Caryophyllaceae through Lardizabalaceae). Science press, Missouri botanical garden press, Beijing, St. Louis, pp 66–100. http://flora.huh.harvard.edu/china/mss/volume06/index.htm. Accessed 8 Mai 2020
Logacheva MD, Samigullin TH, Dhingra A, Penin AA (2008) Comparative chloroplast genomics and phylogenetics of Fagopyrum esculentum ssp. ancestrale - a wild ancestor of cultivated buckwheat. BMC Plant Biol 8:59–59. https://doi.org/10.1186/1471-2229-8-59
McNeill J (1978) Silene alba and S. dioica in North America and the generic delimitation of Lychnis, Melandrium, and Silene (Caryophyllaceae). Can J Bot 56:297–308. https://doi.org/10.1139/b78-037
Melodelima C, Lobréaux S (2013) Complete Arabis alpina chloroplast genome sequence and insight into its polymorphism. Meta Gene 1:65–75. https://doi.org/10.1016/j.mgene.2013.10.004
Mikhaylova YV, Krapivskaya EE, Rodionov AV (2016) Molecular phylogenetic study of Xamilenis Raf. Recognized as the segregate genus in the Sileneae tribe. Russ J Genet Appl Res 6:144–151. https://doi.org/10.1134/S2079059716020052
Morton JK (2005) Silene L. In: Flora of North America editorial committee (ed) Flora of North America. North of Mexico. Volume 5. Magnoliophyta: Caryophyllidae, part 2. Oxford University press, New York, pp 166–220
Nei M, Gojoborit T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3:418–426. https://doi.org/10.1093/oxfordjournals.molbev.a040410
Okonechnikov K, Golosova O, Fursov M (2012) Unipro UGENE: a unified bioinformatics toolkit. Bioinformatics 28:1166–1167. https://doi.org/10.1093/bioinformatics/bts091
Oxelman B, Liden M (1995) Generic boudaries in the tribe Sileneae (Caryophyllaceae) as inferred from nuclear rDNA sequences. Taxon 44:525–542
Oxelman B, Liden M, Rabeler RK, Popp M (2001) A revised generic classification of the tribe Sileneae (Caryophyllaceae). Nord J Bot 20:743–748
Oxelman B, Rautenberg A, Thollesson M et al (2013) Sileneae taxonomy and systematics. http://www.sileneae.info. Accessed 1 Mai 2020
Papadopulos AST, Chester M, Ridout K, Filatov DA (2015) Rapid Y degeneration and dosage compensation in plant sex chromosomes. Proc Natl Acad Sci U S A 112:13021–13026. https://doi.org/10.1073/pnas.1508454112
Park J, Kim Y (2019) The second complete chloroplast genome of Dysphania pumilio (R.Br.) Mosyakin & Clemants (Amranthaceae): intraspecies variation of invasive weeds. Mitochondrial DNA Part B Resour 4:1428–1429. https://doi.org/10.1080/23802359.2019.1598807
Park J, Kim Y, Xi H, Oh YJ, Hahm KM, Ko J (2019) The complete chloroplast genome of common camellia tree in Jeju island, Korea, Camellia japonica L. (Theaceae): intraspecies variations on common camellia chloroplast genomes. Mitochondrial DNA Part B Resour 4:1292–1293. https://doi.org/10.1080/23802359.2019.1591214
R Core Team (2020). R: a language and environment for statistical computing. R Foundation for statistical computing, Vienna. URL https://www.R-project.org/. Accessed 8 Mai 2020
Rautenberg A, Hathaway L, Oxelman B, Prentice HC (2010) Geographic and phylogenetic patterns in Silene section Melandrium (Caryophyllaceae) as inferred from chloroplast and nuclear DNA sequences. Mol Phylogenet Evol 57:978–991
Ronquist F, Teslenko M, Van Der Mark P et al (2012) Software for systematics and evolution MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. https://doi.org/10.1093/sysbio/sys029
Shapiro BJ (2014) Signatures of natural selection and ecological differentiation in microbial genomes. Adv Exp Med Biol:339–359
Shi C, Hu N, Huang H, Gao J, Zhao YJ, Gao LZ (2012) An improved chloroplast DNA extraction procedure for whole plastid genome sequencing. PLoS One 7:e31468. https://doi.org/10.1371/journal.pone.0031468
Shikanai T (2016) Chloroplast NDH: a different enzyme with a structure similar to that of respiratory NADH dehydrogenase. Biochim Biophys Acta Bioenerg 1857:1015–1022. https://doi.org/10.1016/j.bbabio.2015.10.013
Sloan DB, Alverson AJ, Štorchová H, Palmer JD, Taylor DR (2010) Extensive loss of translational genes in the structurally dynamic mitochondrial genome of the angiosperm Silene latifolia. BMC Evol Biol 10:274. https://doi.org/10.1186/1471-2148-10-274
Sloan DB, Alverson AJ, Chuckalovcak JP, Wu M, McCauley DE, Palmer JD, Taylor DR (2012a) Rapid evolution of enormous, multichromosomal genomes in flowering plant mitochondria with exceptionally high mutation rates. PLoS Biol 10:e1001241. https://doi.org/10.1371/journal.pbio.1001241
Sloan DB, Alverson AJ, Wu M, Palner JD, Taylor DR (2012b) Recent acceleration of plastid sequence and structural evolution coincides with extreme mitochondrial divergence in the angiosperm genus Silene. Genome Biol Evol 4:294–306. https://doi.org/10.1093/gbe/evs006
Sloan DB, Triant DA, Forrester NJ, Bergner LM, Wu M, Taylor DR (2014) A recurring syndrome of accelerated plastid genome evolution in the angiosperm tribe Sileneae (Caryophyllaceae). Mol Phylogenet Evol 72:82–89. https://doi.org/10.1016/j.ympev.2013.12.004
Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313. https://doi.org/10.1093/bioinformatics/btu033
Taylor DR, Keller SR (2007) Historical range expansion determines the phylogenetic diversity introduced during contemporary species invasion. Evolution 61:334–345. https://doi.org/10.1111/j.1558-5646.2007.00037.x
Tillich M, Lehwark P, Pellizzer T, Ulbricht-Jones ES, Fisher A, Bock R, Greiner S (2017) GeSeq – versatile and accurate annotation of organelle genomes. Nucleic Acids Res 45:W6–W11. https://doi.org/10.1093/nar/gkx391
Treangen TJ, Ondov BD, Koren S, Phillippy AM (2014) The harvest suite for rapid core-genome alignment and visualization of thousands of intraspecific microbial genomes. Genome Biol 15:524. https://doi.org/10.1186/s13059-014-0524-x
Tzvelev NN (2004) Melandrium Röhl. In: Tzvelev NN (ed) Flora Europae Orientalis. Tomus XI Magnoliophyta: Magnoliopsida Oficina Editoria KMK, Moscua-Petropoli, pp 218-220. [In Russian]
Vaidya G, Lohman DJ, Meier R (2011) SequenceMatrix: concatenation software for the fast assembly of multi-gene datasets with character set and codon information. Cladistics 27:171–180. https://doi.org/10.1111/j.1096-0031.2010.00329.x
Wick RR, Schultz MB, Zobel J, Holt KE (2015) Bandage: interactive visualization of de novo genome assemblies. Bioinformatics 31:3350–3352. https://doi.org/10.1093/bioinformatics/btv383
Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer-Verlag, New York
Wu Z, Tembrock LR (2015) Two complete chloroplast genomes of white campion (Silene latifolia) from male and female individuals. Mitochondrial DNA Part A 28:375–376. https://doi.org/10.3109/19401736.2015.1126829
Yao G, Jin JJ, Li HT, Yang JB, Mandala VS, Croley M, Mostow R, Douglas NA, Chase MW, Christenhusz MJM, Soltis DE, Soltis PS, Smith SA, Brockington SF, Moore MJ, Yi TS, Li DZ (2019) Plastid phylogenomic insights into the evolution of Caryophyllales. Mol Phylogenet Evol 134:74–86. https://doi.org/10.1016/j.ympev.2018.12.023
Acknowledgments
The authors thank Elena Krapivskaja for assistance in plant collecting, Dr. Elena Vojchehovskaya and Dr. Kiril Demchenko for access to some equipment, Dr. Anna Speranskaya for valuable advices about DNA preparation for Illumina sequencing, and Dr. Victoria Schneyer for draft corrections. The research was done using equipment of The Core Facilities Center “Cell and Molecular Technologies in Plant Science” at the Komarov Botanical Institute RAS and Center “Biobank” at the Research Park of St. Petersburg State University (St. Petersburg, Russia).
Funding
The research was supported by Russian Foundation for Basic Research (RFBR) Grant for Young Researchers # 16-34-01024 obtained by YM (all laboratory work), RFBR Grant # 18-04-01040 (field work), partially by SPbSU Grant 60256916 (bioinformatics and manuscript preparation) for AR.
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Yulia Mikhaylova and Alexander Rodionov contributed to the study conception and design. Elisaveta Punina collected plant material. Dmitrii Polev and Anna Maslova performed NGS library preparation and sequencing. Yulia Mikhaylova made chloroplast DNA enrichment, NGS data analysis and wrote the draft of the manuscript. Mikhail Gordon made a phylogenetic analysis. Alexander Rodionov edited and critically revised manuscript. All authors read and approved the final manuscript.
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Key Message
• Plastome of Silene latifolia subsp. alba collected in native range in Eastern Europe was sequenced.
• High levels of SNPs indicate high genetic plasticity of the species and contribute to its invasive success
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Mikhaylova, Y.V., Gordon, M., Maslova, A.R. et al. Chloroplast Genome of Native Silene latifolia subsp. alba from Fennoscandia Shows High Level of Differences from Invasive White Campion. Plant Mol Biol Rep 39, 226–239 (2021). https://doi.org/10.1007/s11105-020-01246-7
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DOI: https://doi.org/10.1007/s11105-020-01246-7