Abstract
We provide here the first full chloroplast genome sequence, i.e., the plastome, for a species belonging to the fern order Hymenophyllales. The phylogenetic position of this order within leptosporangiate ferns, together with the general scarcity of information about fern plastomes, places this research as a valuable study on the analysis of the diversity of plastomes throughout fern evolution. Gene content of V. speciosa plastome was similar to that in most ferns, although there were some characteristic gene losses and lineage-specific differences. In addition, an important number of genes required U to C RNA editing for proper protein translation and two genes showed start codons alternative to the canonical AUG (AUA). Concerning gene order, V. speciosa shared the specific 30-kb inversion of euphyllophytes plastomes and the 3.3-kb inversion of fern plastomes, keeping the ancestral gene order shared by eusporangiate and early leptosporangiate ferns. Conversely, V. speciosa has expanded IR regions comprising the rps7, rps12, ndhB and trnL genes in addition to rRNA and other tRNA genes, a condition shared with several eusporangiate ferns, lycophytes and hornworts, as well as most seed plants.
Similar content being viewed by others
References
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410
Ben-Menni Schuler SBM, García-López MC, López-Flores I, Nieto-Lugilde M, Suárez-Santiago VN (2017) Genetic diversity and population history of the Killarney fern, Vandenboschia speciosa (Hymenophyllaceae), at its southern distribution limit in continental Europe. Bot J Linn Soc 183:94–105
Brázda V, Laister RC, Jagelská EB, Arrowsmith C (2011) Cruciform structures are a common DNA feature important for regulating biological processes. BMC Mol Biol 12:33
Chaw SM, Chang CC, Chen HL, Li WH (2004) Dating the monocot-dicot divergence and the origin of core eudicots using whole chloroplast genomes. J Mol Evol 58:424–441
Chumley TW, Palmer JD, Mower JP, Fourcade HM, Calie PJ, Boore JL, Jansen RK (2006) The complete chloroplast genome sequence of Pelargonium × hortorum: organization and evolution of the largest and most highly rearranged chloroplast genome of land plants. Mol Biol Evol 23:2175–2190
Drescher A, Ruf S, Calsa T, Carrer H, Bock R (2000) The two largest chloroplast genome encoded open reading frames of higher plants are essential genes. Plant J 22:97–104
Dubuisson J-Y, Hennequin S, Douzery EJP, Cranfill RB, Smith AR, Pryer KM (2003) rbcL phylogeny of the fern genus Trichomanes (Hymenophyllaceae), with special reference to neotropical taxa. Int J Plant Sci 164:753–761
Duffy AM, Kelchner SA, Wolf PG (2009) Conservation of selection on matK following an ancient loss of its flanking intron. Gene 438:17–25
Ebihara A, Iwatsuki K, Ito M, Hennequin S, Dubuisson J-Y (2007) A global molecular phylogeny of the fern genus Trichomanes (Hymenophyllaceae) with special reference to stem anatomy. Bot J Linnean Society 155:1–27
Gantt JS, Baldauf SL, Calie PJ, Weeden NF, Palmer JD (1991) Transfer of rpl22 to the nucleus greatly preceded its loss from the chloroplast and involved the gain of an intron. EMBO J 10:3073–3078
Gao L, Yi X, Yang Y-X, Su Y-J, Wang T (2009) Complete chloroplast genome sequence of a tree fern Alsophila spinulosa: insights into evolutionary changes in fern chloroplast genomes. BMC Evol Biol 9:130
Gao L, Su Y-J, Wang T (2010) Plastid genome sequencing, comparative genomics, and phylogenomics: current status and prospects. J Syst Evol 48:77–93
Gao L, Zhou Y, Wang Z-W, Su Y-J, Wang T (2011) Evolution of the rpoB-psbZ region in fern plastid genomes: notable structural rearrangements and highly variable intergenic spacers. BMC Plant Biol 11:64
Gao L, Wang B, Wang Z-W, Zhou Y, Su Y-J, Wang T (2013) Plastome sequences of Lygodium japonicum and Marsilea crenata reveal the genome organization transformation from basal ferns to core leptosporangiates. Genome Biol Evol 5:1403–1407
Green BR (2011) Chloroplast genomes of photosynthetic eukaryotes. Plant J 66:34–44
Grewe F, Guo W, Gubbels EA, Hansen AK, Mower JP (2013) Complete plastid genomes from Ophioglossum californicum, Psilotum nudum, and Equisetum hyemale reveal an ancestral land plant genome structure and resolve the position of Equisetales among monilophytes. BMC Evol Biol 13:8
Groth-Malonek M, Wahrmund U, Polsakiewicz M, Knoop V (2007) Evolution of a pseudogene: exclusive survival of a functional mitochondrial nad7 gene supports Haplomitrium as the earliest liverwort lineage and proposes a secondary loss of RNA editing in Marchantiidae. Mol Biol Evol 24:1068–1074
Guisinger MM, Kuehl JV, Boore JL, Jansen RK (2011) Extreme reconfiguration of plastid genomes in the angiosperm family Geraniaceae: rearrangements, repeats, and codon usage. Mol Biol Evol 28:583–600
Guo W, Grewe F, Cobo-Clark A, Fan W, Duan Z, Adams RP, Schwarzbach AE, Mower JP (2014) Predominant and substoichiometric isomers of the plastid genome coexist within Juniperus plants and have shifted multiple times during cupressophyte evolution. Genome Biol Evol 6:580–590
Guo W, Grewe F, Mower JP (2015) Variable frequency of plastid RNA editing among ferns and repeated loss of uridine-to-cytidine editing from vascular plants. PLoS One 10:e0117075
Guo Z-Y, Zhang H-R, Shrestha N, Zhang X-C (2016) Complete chloroplast genome of a valuable medicinal plant, Huperzia serrata (Lycopodiaceae), and comparison with its congener. Appl Plant Sci 4:1600071
Haberle RC, Fourcade HM, Boore JL, Jansen RK (2008) Extensive rearrangements in the chloroplast genome of Trachelium caeruleum are associated with repeats and tRNA genes. J Mol Evol 66:350–361
Hahn C, Bachmann L, Chevreux B (2013) Reconstructing mitochondrial genomes directly from genomic next-generation sequencing reads—a baiting and iterative mapping approach. Nucleic Acids Res 41:e129
Hasebe M, Iwatsuki K (1990) Chloroplast DNA from Adiantum capillus-veneris L., a fern species (Adiantaceae); clone bank, physical map and unusual gene localization in comparison with angiosperm chloroplast DNA. Curr Genet 17:359–364
Hasebe M, Iwatsuki K (1992) Gene localization on the chloroplast DNA of the maiden hair fern, Adiantum capillus-veneris. J Plant Res 105:413–419
Hausner G, Olson R, Simon D, Johnson I, Sanders ER, Karol KG, McCourt RM, Zimmerly S (2006) Origin and evolution of the chloroplast trnK (matK) intron: a model for evolution of group II intron RNA structures. Mol Biol Evol 23:380–391
Inagaki H, Ohye T, Kogo H, Tsutsumi M, Kato T, Tong M, Emanuel BS, Kurahashi H (2013) Two sequential cleavage reactions on cruciform DNA structures cause palindrome-mediated chromosomal translocations. Nature Commun 4:1592
Jansen RK, Cai Z, Raubeson LA et al (2007) Analysis of 81 genes from 64 plastid genomes resolves relationships in angiosperms and identifies genome-scale evolutionary patterns. Proc Natl Acad Sci USA 104:19369–19374
Jansen RK, Saski C, Lee S, Hansen AK, Daniell H (2011) Complete plastid genome sequences of three rosids (Castanea, Prunus, Theobroma): evidence for at least two independent transfers of rpl22 to the nucleus. Mol Biol Evol 28:835–847
Karol KG, Arumuganathan K, Boore JL, Duffy AM, Everett KDE, Hall JD, Hansen SK, Kuehl JV, Mandoli DF, Mishler BD, Olmstead RG, Renzaglia KS, Wolf PG (2010) Complete plastome sequences of Equisetum arvense and Isoetes flaccida: implications for phylogeny and plastid genome evolution of early land plant lineages. BMC Evol Biol 10:321
Kearse MG, Wilusz JE (2017) Non-AUG translation: a new start for protein synthesis in eukaryotes. Genes Dev 31:1717–1731
Keller J, Rousseau-Gueutin M, Martin GE, Morice J, Boutte J, Coissac E, Ourari M, Aïnouche M, Salmon A, Cabello-Hurtado F, Aïnouche A (2017) The evolutionary fate of the chloroplast and nuclear rps16 genes as revealed through the sequencing and comparative analyses of four novel legume chloroplast genomes from Lupinus. DNA Res 24:343–358
Kim HT, Chung MG, Kim K-J (2014) Chloroplast genome evolution in early diverged leptosporangiate ferns. Mol Cells 37:372–382
Knie N, Fischer S, Grewe F, Polsakiewicz M, Knoop V (2015) Horsetails are the sister group to all other monilophytes and Marattiales are sister to leptosporangiate ferns. Mol Phyl Evol 90:140–149
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 Evol Biol 16:134
Kolb J, Chuzhanova NA, Högel J, Vasquez KM, Cooper DN, Bacolla A, Kehrer-Sawatzki H (2009) Cruciform-forming inverted repeats appear to have mediated many of the microinversions that distinguish the human and chimpanzee genomes. Chromosome Res 17:469–483
Kugita M, Yamamoto Y, Fujikawa T, Matsumoto T, Yoshinaga K (2003) RNA editing in hornwort chloroplasts makes more than half the genes functional. Nucleic Acids Res 31:2417–2423
Kuo LY, Li FW, Chiou WL, Wang CN (2011) First insights into fern matK phylogeny. Mol Phyl Evol 59:556–566
Kuroda H, Suzuki H, Kusumegi T, Hirose T, Yukawa Y, Sugiura M (2007) Translation of psbC mRNAs starts from the downstream GUG, not the upstream AUG, and requires the extended Shine–Dalgarno sequence in tobacco chloroplasts. Plant Cell Physiol 48:1374–1378
Labiak PH, Karol KG (2017) Plastome sequences of an ancient fern lineage reveal remarkable changes in gene content and architecture. Am J Bot 104:1008–1018
Langmead B, Salzberg S (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359
Laslett D, Canback B (2004) ARAGORN, a program for the detection of transfer RNA and transfer-messenger RNA genes in nucleotide sequences. Nucleic Acids Res 32:11–16
Lehtonen S (2011) Towards resolving the complete fern tree of life. PLoS One 6:e24851
Logacheva MD, KrinitsinaAA, Belenikin MS, Khafizov K, Konorov EA, Kuptsov SV, Speranskaya AS (2017) Comparative analysis of inverted repeats of polypod fern (Polypodiales) plastomes reveals two hypervariable regions. Plant Biol 17:255
Lohse M, Drechsel O, Kahlau S, Bock R (2013) OrganellarGenomeDRAW—a suite of tools for generating physical maps of plastid and mitochondrial genomes and visualizing expression data sets. Nucleic Acids Res 41:W575–W581
Lowe TM, Chan PP (2016) tRNAscan-SE on-line: search and contextual analysis of transfer RNA genes. Nucleic Acids Res 44:W54–W57
Lu J-M, Zhang N, Du X-Y, Wen J, Li D-Z (2015) Chloroplast phylogenomics resolves key relationships in ferns. J Syst Evol 53:448–457
Novák P, Neumann P, Pech J, Steinhaisl J, Macas J (2013) RepeatExplorer: a galaxy-based web server for genome-wide characterization of eukaryotic repetitive elements from next-generation sequence reads. Bioinformatics 29:792–793
Obermayer R, Leitch IJ, Hanson L, Bennett MD (2002) Nuclear DNA C-values in 30 species double the familial representation in pteridophytes. Ann Bot 90:209–217
Park M, Park H, Lee H, Lee B, Lee J (2018) The complete plastome sequence of an Antarctic bryophyte Sanionia uncinata (Hedw.) Loeske. Int J Mol Sci 19:709
Pfitzinger H, Weil JH, Pillay DT, Guillemaut P (1990) Codon recognition mechanisms in plant chloroplasts. Plant Mol Biol 14:805–814
PPG I (2016) A community-derived classification for extant lycophytes and ferns. J Syst Evol 54:563–603
Pryer KM, Schneider H, Smith AR, Cranfill R, Wolf PG, Hunt JS, Sipes SD (2001) Horsetails and ferns are a monophyletic group and the closest living relatives to seed plants. Nature 409:618–622
Pryer KM, Schuettpelz E, Wolf PG, Schneider H, Smith AR, Cranfill R (2004) Phylogeny and evolution of ferns (monilophytes) with a focus on the early leptosporangiate divergences. Am J Bot 91:1582–1598
Qi X, Kuo L-Y, Guo C, Li H, Li Z et al (2018) A well-resolved fern nuclear phylogeny reveals the evolution history of numerous transcription factor families. Mol Phylogenet Evol 127:961–977
Rai HS, Graham SW (2010) Utility of a large, multigene plastid data set in inferring higher-order relationships in ferns and relatives (monilophytes). Am J Bot 97:1444–1456
Raubeson LA, Jansen RK (1992) Chloroplast genomes of plants. In: Henry RJ (ed) Plant diversity and evolution: genotypic and phenotypic variation in higher plants. CABI Publishing, London, pp 45–68
Rice P, Longden I, Bleasby A (2000) EMBOSS: the european molecular biology open software suite. Trends Genet 16:276–277
Roper JM, Hansen SK, Wolf PG, Karol KG, Mandoli DF, Everett KDE, Kuehl J, Boore JL (2007) The complete plastid genome sequence of Angiopteris evecta (G. Forst.) Hoffm. (Marattiaceae). Am Fern J 97:95–106
Rothfels CJ, Li F-W, Sigel EM, Huiet L, Larsson A et al (2015) The evolutionary history of ferns inferred from 25 low-copy nuclear genes. Am J Bot 102:1089–1107
Rüdinger M, Volkmar U, Lenz H, Groth-Malonek M, Knoop V (2012) Nuclear DYW-type PPR gene families diversify with increasing RNA editing frequencies in liverwort and moss mitochondria. J Mol Evol 74:37–51
Ruhlman TA, Jansen RK (2014) The plastid genomes of flowering plants. In: Maliga P (ed) Chloroplast biotechnology: methods and protocols. Methods in molecular biology, vol 1132. Springer Science + Business Media, New York, pp 3–38
Rumsey FJ, Vogel JC, Russell SJ, Barrett JA, Gibby M (1999) Population genetics and conservation biology of the endangered fern Trichomanes speciosum (Hymenophyllaceae) in Scotland. Biol J Linn Soc 66:333–344
Schuettpelz E, Pryer KM (2007) Fern phylogeny inferred from 400 leptosporangiate species and three plastid genes. Taxon 56:1037–1050
Smith AR, Pryer KM, Schuettpelz E, Korall P, Schneider H, Wolf PG (2006) A classification for extant ferns. Taxon 55:705–731
Song M, Kuo L-Y, Huiet L, Pryer KM, Rothfels CJ, Li F-W (2018) A novel chloroplast gene reported for flagellate plants. Am J Bot 105:117–121
Sugiura M (2008) RNA editing in chloroplasts. In: Göringer HU (ed) RNA editing. Nucleic acids and molecular biology, vol 20. Springer, Berlin
Sun Y, Moore MJ, Zhang S, Soltis PS, Soltis DE, Zhao T, Meng A, Li X, Li J, Wang H (2016) Phylogenomic and structural analyses of 18 complete plastomes across nearly all families of early-diverging eudicots, including an angiosperm-wide analysis of IR gene content evolution. Mol Phylogenet Evol 96:93–101
Thorvaldsdóttir H, Robinson JT, Mesirov JP (2013) Integrative genomics viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform 14:178–192
Tillich M, Lehwark P, Pellizzer T, Ulbricht-Jones ES, Fischer A, Bock R, Greiner S (2017) GeSeq—versatile and accurate annotation of organelle genomes. Nucleic Acids Res 45:W6–W11
Tsuji S, Ueda K, Nishiyama T, Hasebe M, Yoshikawa S, Konagaya A, Nishiuchi T, Yamaguchi K (2007) The chloroplast genome from a lycophyte (microphyllophyte), Selaginella uncinata, has a unique inversion, transpositions and many gene losses. J Plant Res 120:281–290
Wicke S, Quandt D (2009) Universal primers for the amplification of the plastid trnK/matK region in land plants. Anales Jard Bot Madrid 66:285–288
Wicke S, Schneeweiss GM, dePamphilis CW, Müller KF, Quandt D (2011) The evolution of the plastid chromosome in land plants: gene content, gene order, gene function. Plant Mol Biol 76:273–297
Wolf PG, Karol KG (2012) Plastomes of bryophytes, lycophytes and ferns. In: Bock R, Knoop V (eds) Advances in photosynthesis and respiration. Genomics of chloroplasts and mitochondria, vol 35. Springer, Dordrecht, pp 89–102
Wolf PG, Rowe CA, Sinclair RB, Hasebe M (2003) Complete nucleotide sequence of the chloroplast genome from a leptosporangiate fern, Adiantum capillus-veneris L. DNA Res 10:59–65
Wolf PG, Rowe CA, Hasebe M (2004) High levels of RNA editing in a vascular plant chloroplast genome: analysis of transcripts from the fern Adiantum capillus-veneris. Gene 339:89–97
Wolf PG, Karol KG, Mandolib DF, Kuehld J, Arumuganathane K, Ellisa MW, Mishler BD, Kelchf DG, Olmstead RG, Boore JL (2005) The first complete chloroplast genome sequence of a lycophyte, Huperzia lucidula (Lycopodiaceae). Gene 350:117–128
Wolf PG, Roper JM, Duffy AM (2010) The evolution of chloroplast genome structure in ferns. Genome 53:731–738
Wyman SK, Jansen RK, Boore JL (2004) Automatic annotation of organellar genomes with DOGMA. Bioinformatics 20:3252–3255
Xu J-H, Liu Q, Hua W, Wang T, Xue Q, Messing J (2015) Dynamics of chloroplast genomes in green plants. Genomics 106:221–231
Zhong B, Fong R, Collins LJ, McLenachan PA, Penny D (2014) Two new fern chloroplasts and decelerated evolution linked to the long generation time in tree ferns. Genome Biol Evol 6:1166–1173
Zhu A, Guo W, Gupta S, Fan W, Mower JP (2016) Evolutionary dynamics of the plastid inverted repeat: the effects of expansion, contraction, and loss on substitution rates. New Phytol 209:1747–1756
Acknowledgements
This research has been financed by the Spanish Ministerio de Economía y Competitividad and FEDER founds, Grant: CGL2010-14856 (subprograma BOS). The Dirección General de Gestión del Medio Natural y Espacios Protegidos of the Consejería de Medio Ambiente y Ordenación del Territorio de la Junta de Andalucía authorized and facilitates the sampling of the material. We are highly indebted to Carmen Rodríguez Hiraldo and to Jaime Pereña Ortiz who, together with the team of Agentes de Medio Ambiente of the Consejería, helped us with the sampling procedure.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Ruiz-Ruano, F.J., Navarro-Domínguez, B., Camacho, J.P.M. et al. Full plastome sequence of the fern Vandenboschia speciosa (Hymenophyllales): structural singularities and evolutionary insights. J Plant Res 132, 3–17 (2019). https://doi.org/10.1007/s10265-018-1077-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10265-018-1077-y