Abstract
We determined the complete nucleotide sequence of the chloroplast genome of Selaginella uncinata, a lycophyte belonging to the basal lineage of the vascular plants. The circular double-stranded DNA is 144,170 bp, with an inverted repeat of 25,578 bp separated by a large single copy region (LSC) of 77,706 bp and a small single copy region (SSC) of 40,886 bp. We assigned 81 protein-coding genes including four pseudogenes, four rRNA genes and only 12 tRNA genes. Four genes, rps15, rps16, rpl32 and ycf10, found in most chloroplast genomes in land plants were not present in S. uncinata. While gene order and arrangement of the chloroplast genome of another lycophyte, Hupertzia lucidula, are almost the same as those of bryophytes, those of S. uncinata differ considerably from the typical structure of bryophytes with respect to the presence of a unique 20 kb inversion within the LSC, transposition of two segments from the LSC to the SSC and many gene losses. Thus, the organization of the S. uncinata chloroplast genome provides a new insight into the evolution of lycophytes, which were separated from euphyllophytes approximately 400 million years ago.
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Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402
Bendich AJ (2004) Circular chloroplast chromosomes: the grand illusion. Plant Cell 16:1661–1666
Cai X, Fuller AL, McDougald LR, Zhu G (2003) Apicoplast genome of the coccidian Eimeria tenella. Gene 321:39–46
Delage L, Duchene A-M, Zaepfel M, Maréchal-Drouard L (2003) The anticodon and the D-domain sequences are essential determinants for plant cytosolic tRNAVal import into mitochondria. Plant J 34:623–633
Doyle JJ, Davis JI, Soreng RJ, Garvin D, Anderson MJ (1992) Chloroplast DNA inversions and the origin of the grass family (Poaceae). Proc Natl Acad Sci USA 89:7723–7726
Ewing B, Green P (1998) Basecalling of automated sequencer traces using phred. II. Error probabilities. Genome Res 8:186–194
Ewing B, Hillier L, Wendl M, Green P (1998) Basecalling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res 8:175–185
Gifford EM, Foster AS (1989) Morphology and evolution of vascular plants. Freeman, New York
Glover KE, Spencer DF, Gray MW (2001) Identification and structural characterization of nucleus-encoded transfer RNAs imported into wheat mitochondria. J Biol Chem 276:639–648
Hasebe M, Iwatsuki K (1992) Gene localization on the chloroplast DNA of the maiden hair fern; Adiantum capillus-veneris. Bot Mag Tokyo 105:413–419
Hiratsuka J, Shimada H, Whittier R, Ishibashi T, Sakamoto M, Mori M, Kondo C, Honji Y, Sun CR, Meng BY, Li YQ, Kanno A, Nishizawa Y, Hirai A, Shinozaki K, Sugiura M (1989) The complete sequence of the rice (Oryza sativa) chloroplast genome: intermolecular recombination between distinct tRNA genes accounts for a major plastid DNA inversion during the evolution of the cereals. Mol Gen Genet 217:185–194
Hirose T, Sugiura M (2001) Involvement of a site-specific trans-acting factor and a common RNA-binding protein in the editing of chloroplast mRNAs: development of a chloroplast in vitro RNA editing system. EMBO J 20:1144–1152
Kato T, Kaneko T, Sato S, Nakamura Y, Tabata S (2000) Complete structure of the chloroplast genome of a legume, Lotus japonicus. DNA Res 7:323–330
Kenrick P, Crane PR (1997) The origin and early evolution of plants on land. Nature 389:33–39
Kim KJ, Lee HL (2004) Complete chloroplast genome sequences from Korean ginseng (Panax schinseng Nees) and comparative analysis of sequence evolution among 17 vascular plants. DNA Res 11:247–261
Kugita M, Kaneko A, Yamamoto Y, Takeya Y, Matsumoto T, Yoshinaga K (2003a) The complete nucleotide sequence of the hornwort (Anthoceros formosae) chloroplast genome: insight into the earliest land plants. Nucleic Acids Res 31:716–721
Kugita M, Yamamoto Y, Fujikawa T, Matsumoto T, Yoshinaga K (2003b) RNA editing in hornwort chloroplasts makes more than half the genes functional. Nucleic Acids Res 31:2417–2423
Lidholm J, Szmidt A, Gustafsson P (1991) Duplication of the psbA gene in the chloroplast genome of two Pinus species. Mol Gen Genet 226:345–352
Lowe TM, Eddy SR (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25:955–964
Maier BD, Neckerman K, Igloi GL, Kossel H (1995) Complete sequence of the maize chloroplast genome: gene content, hotspots of divergency and fine tuning of genetic information by transcript editing. J Mol Biol 251:614–628
Maréchal-Drouard L, Weil JH, Dietrich A (1993) Transfer RNAs and transfer RNA genes in plants. Annu Rev Plant Physiol 44:13–32
Morden CW, Wolfe K., dePamphilis CW, Palmer JD (1991) Plastid translation and transcription genes in a non-photosynthetic plant: intact, missing and pseudo genes. EMBO J 10:3281–3288
Ohyama K, Fukazawa H, Kohchi T, Shirai H, Sano T, Sano S, Umesono K, Shiki Y, Takeuchi M, Chang Z, Aota S, Inokuchi H, Ozeki H (1986) Chloroplast gene organization deduced from complete sequence of liverwort Marchantia polymorpha chloroplast DNA. Nature 322:572–574
Palmer JD (1991) Plastid chromosomes: structure and evolution. In: Hermann RG (ed) The molecular biology of plastids. Cell culture and somatic cell genetics of plants, vol. 7a. Springer, Vienna Berlin Heidelberg, pp 5–53
Palmer JD, Stein DB (1986) Conservation of chloroplast genome structure among vascular plants. Curr Genet 10:823–833
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
Raubeson LA, Jansen RK (1992) Chloroplast DNA evidence on the ancient evolutionary split in vascular land plants. Science 255:1697–1699
Raubeson LA, Jansen RK (2005) Chloroplast genomes of plants. In: Henry RJ (ed) Plant diversity and evolution: genotypic variation in higher plants. CAB International, Wallingford, UK, pp 45–68
Saltz Y, Beckman J (1981) Chloroplast DNA preparation from Petunia and Nicotiana. Plant Mol Biol Newsl 2:73–74
Shinozaki K, Ohme M, Tanaka M, Wakasugi T. Hayashida N, Matsubayashi T, Zaita N, Chunwongse J, Obokata J, Yamaguchi-Shinozaki K, Ohto C, Torazawa K, Meng BY, Sugita M, Deno H, Kamogashira T, Yamada K, Kusuda J, Takaiwa F, Kato A, Tohdoh N, Shimada H, Sugiura M (1986) The complete nucleotide sequence of tobacco chloroplast genome: its gene organization and expression. EMBO J 5:2043–2049
Stein DB, Conant DS, Ahearn ME, Jordan ET, Kirch SA, Hasebe M, Iwatsuki K, Tan MK, Thomson JA (1992) Structural rearrangements of the chloroplast genome provide an important phylogenetic link in ferns. Proc Natl Acad Sci USA 89:1856–1860
Sugiura M (1992) The chloroplast genome. Plant Mol Biol 19:149–168
Sugiura C, Kobayashi Y, Aoki S, Sugita C, Sugita M (2003) Complete chloroplast DNA sequence of the moss Physcomitrella patens: evidence for the loss and relocation of rpoA from the chloroplast to the nucleus. Nucleic Acids Res 31:5324–5331
Takamiya M (1993) Comparatative karyomorphology and interrelationships of Selaginella in Japan. J Plant Res 106:149–166
Tillich M, Funk HT, Schmitz-Linneweber C, Poltnigg P, Sabater B, Martin M, Maier RM (2005) Editing of plastid RNA in Arabidopsis thaliana ecotypes. Plant J 43:708–715
Turmel M, Otis C, Lemieux C (1999) The complete chloroplast DNA sequence of the green alga Nephroselmis olivacea insights into the architecture of ancestral chloroplast genomes. Proc Natl Acad Sci USA 96:10248–10253
Wakasugi T, Tsudzuki J, Ito S, Nakashima K, Tsudzuki T, Sugiura M (1994) Loss of all ndh genes as determined by sequencing the entire chloroplast genome of the black pine Pinus thunbergii. Proc Natl Acad Sci USA 91:9794–9798
Wakasugi T, Hirose T, Horihata M, Tsudzuki T, Kossel H, Sugiura M (1996) Creation of a novel protein-codong region at the RNA level in black pine chloroplast: the pattern of RNA editing in the gymnosperm chloroplast is different from that in angiosperms. Proc Natl Acad Sci USA 93:8766–8770
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, Karol KG, Mandoli DF, Kuehl J, Arumuganathan K, Ellis MW, Mishler BD, Kelch DG, Olmstead RG, Boore JL (2005a) The first complete chloroplast genome sequence of a lycophyte, Huperzia lucidula (Lycopodiaceae). Gene 350:117–128
Wolf PG, Rowe CA, Hasebe M (2005b) High levels of RNA editing in a vascular plant chloroplast genome: analysis of transcripts from the fern Adiantum capillus-veneris. Gene 339:89–97
Zaita N, Torazawa K, Shinozaki K, Sugiura M (1987) Trans splicing in vivo: joining of transcripts from the ‘divided’ gene for ribosomal protein S12 in the chloroplasts of tobacco. FEBS Lett 210:153–156
Acknowledgments
We are very grateful to Prof. M. Takamiya for cytogenetical observations of S. uncinata. We also thank T. Hoshino for drawing the chromosome map and H. Mizuno for technical assistance with DNA sequencing.
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Tsuji, S., Ueda, K., Nishiyama, T. et al. The chloroplast genome from a lycophyte (microphyllophyte), Selaginella uncinata, has a unique inversion, transpositions and many gene losses. J Plant Res 120, 281–290 (2007). https://doi.org/10.1007/s10265-006-0055-y
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DOI: https://doi.org/10.1007/s10265-006-0055-y