436–438 Nucleic Acids Research, 2003, Vol. 31, No. 1 # 2003 Oxford University Press DOI: 10.1093/nar/gkg080

PLMItRNA, a database on the heterogeneous genetic origin of mitochondrial tRNA genes and tRNAs in photosynthetic eukaryotes

Guglielmo Rainaldi, Mariateresa Volpicella, Flavio Licciulli1, Sabino Liuni1, Raffaele Gallerani and Luigi R. Ceci1,*

Dipartimento di Biochimica e Biologia Molecolare, Universita` di Bari and 1Centro di Studio sui Mitocondri e Downloaded from https://academic.oup.com/nar/article/31/1/436/2401376 by guest on 30 September 2021 Metabolismo Energetico, CNR, Via Amendola 165/A, 70126 Bari Italy

Received September 13, 2002; Accepted September 20, 2002

ABSTRACT classification in different classes as indicated in Table 1 for and in a similar Table (see Table S3 in The updated version of PLMItRNA reports informa- Supplementary Material) for Cryptophyta, Rhodophyta and tion and multialignments on 609 genes and 34 tRNA Stramenopiles. These tables report a general view of all the molecules active in the mitochondria of Viridiplantae complete tRNA genes and molecules identified in the (27 Embryophyta and 10 ), and photo- mitochondrial genomes of photosynthetic eukaryotes. synthetic (one Cryptophyta, four Rhodophyta Coloured squares have hyper-textual link to single gene (or and two Stramenopiles). Colour-code based tables molecule) entry. Colour code refers to the different genetic reporting the different genetic origin of identified origin of tRNA genes or molecules (see Table 1). Genes or genes allow hyper-textual link to single entries. molecules with chloroplast or nuclear origins are aligned Promoter sequences identified for tRNA genes in separately. the mitochondrial genomes of Angiospermae are PLMItRNA updating was carried out essentially as already also reported. The PLMItRNA database is accessible described in the previous version (1). More details on the organization of the database and how to at http://bighost.area.ba.cnr.it/PLMItRNA/. retrieve list of specific entries can be found at the PLMItRNA home page: http://bighost.area.ba.cnr.it/PLMItRNA/.

INTRODUCTION PROMOTERS FOR tRNA GENES TRANSCRIPTION PLMItRNA is a database dedicated to the distribution of tRNA In the current version of PLMItRNA a list of promoter genes and molecules in the mitochondria of photosynthetic sequences identified for tRNA genes in mitochondria of eukaryotes (1). With the possible exceptions of Prototheca Angiosperms has been introduced, which could be useful for wickerhamii (2) and Nephroselmis olivacea (3), the genomes studies on the activation of foreign genes in the mitochondrial of these organelles do not code for a complete set of tRNAs. genomes. It is still a matter of investigation how the Missing tRNAs must therefore be imported from the mitochondrial transcription machinery can recognize the cytoplasm. In the case of angiosperms, the presence of tRNA chloroplast sequences to be transcribed. Transcription of cp- genes with different genetic origins (the original endosymbiont tRNA genes in mitochondrial genomes may be occurred owing and chloroplast) can also be observed (4). The puzzling to insertion downstream of pre-existing promoters, or thanks to distribution of active tRNAs in the mitochondria of photo- evolutive rearrangements of their 50-flanking regions which synthetic organisms is therefore the result of a selective process originated functional promoters. A consensus promoter of recruitment of genes and molecules occurred during sequence has been described for angiosperm mitochondrial evolution. genes which shows little differences between monocotyledons Each entry in PLMItRNA reports information on the and dicotyledons (4,5). Promoter consensus is characterized by sequence and organism, useful to retrieve specific lists of a highly conserved tetranucleotide motif, CRTA, that in entries by SRS at http://bighost.area.ba.cnr.it/srs6/. monocots can diverge to TRTA, YYTA or RRTA. The Multialignments of sequences have been divided in four tetranucleotide is part of a larger sequence, usually located at groups, corresponding to Viridiplantae (Chlorophyta/ position from À7toþ2 with respect to the transcription start Embryophyta group) and to the three divisions of algae site. Apparently the same kind of promoters are used in the Cryptophyta, Rhodophyta and Stramenopiles. Within these transcription of protein, ribosomal and tRNA genes (5). Table four groups sequences are reported according to their 2 reports promoter sequences described for tRNA genes in

*To whom correspondence should be addressed. Tel: þ39 0805443311; Fax: þ39 805443317; Email: [email protected] Table 1. Genes coding for mitochondrial tRNAs in Viridiplantae Downloaded fromhttps://academic.oup.com/nar/article/31/1/436/2401376bygueston30September2021 uli cd eerh 03 o.3,N.1 No. 31, Vol. 2003, Research, Acids Nucleic

Full names for plants and algae are reported in Table S1 (Supplementary Material). B: Bryophyta,P:Pedinophyceae, Prasin.: Prasinophyceae,T:,M:Marchantiopsida, 437 C: Coniferopsida. Coloured squares indicated mitochondrial genes (j), chloroplast genes (j), nuclear genes (j) and imported tRNAs (u). 438 Nucleic Acids Research, 2003, Vol. 31, No. 1

Table 2. Promoter sequences identified for tRNA genes in angiosperm mitochondrial genomes

Gene Plant Class Origin Promoter sequence Apex Evidence Ref. trnE(TTC) Sunflower Dicot Mt TTCGTATACGTATAGAAAG Exp. (6) trnF(GAA) Oenothera Dicot Mt -TTAATTTCATAAGAGAGA Exp. (7) trnfM(CAT) A.thaliana Dicot Mt TGAAATATCGTAAGAGAAG Seq. an. Y08501 trnfM(CAT) Maize Monocot Mt -GAATTGACATAGATAAA- Seq. an. (8) trnfM(CAT) Rice Monocot Mt -CAGAAAACGTATAAAAA- Seq. an. (9) trnfM(CAT) Rye Monocot Mt -GAATTGACATAGAGAAA- Seq. an. (8) trnfM(CAT) Wheat Monocot Mt -GAATTGACATAGAGAAA- Seq. an. (8) trnH(GTG) Rice Monocot Cp GGATTATACGTATGTAAA- Exp. (10) trnN(GTT) Potato Dicot Cp -CAAATGGCATAGTATTAG Exp. (4) trnS(GCT) A.thaliana Dicot Mt TACAATTTCATAAGAGAAG Seq. an. Y08501

trnY(GTA) A.thaliana Dicot Mt TAAAATATCATAAGAGAAG Seq. an. Y08501 Downloaded from https://academic.oup.com/nar/article/31/1/436/2401376 by guest on 30 September 2021

aSequences are aligned according to the consensus motif CRTA (bold). Transcription start site is underlined. Exp.: Experimentally determined, Seq. an.: Deduced by sequence analysis. The genetic origin of genes is indicated: Mt (Mitochondrial),Cp (Chloroplast). angiosperm mitochondria as experimentally determined or 4. Hoffmann,M., Kuhn,J., Daschner,K. and Binder,S. (2001) The RNA world deduced by sequence comparison. of plant mitochondria. Prog. Nucleic Acid Res., 70, 119–154. 5. Fey,J. and Marechal-Drouard,L. (1999) Compilation and analysis of plant mitochondrial promoter sequences: an illustration of a divergent evolution between monocot and dicot mitochondria. Biochem. Biophys. Res. Comm., SUPPLEMENTARY MATERIAL 256, 409–414. Supplementary tables on the database are available at NAR 6. Damiano,F., Ceci,L.R., Siculella,L. and Gallerani,R. (2002) Transcription of two sunflower (Helianthus annuus L.) mitochondrial tRNA genes Online. having different genetic origins. Gene, 286,25–32. 7. Binder,S. and Brennicke,A. (1993) A tRNA gene transcription initiation site is similar to mRNA and rRNA promoters in plant mitochondria. REFERENCES Nucleic Acids Res., 21, 5012–5019. 8. Coulthart,M.B., Spencer,D. and Gray,M.W. (1993) Comparative analysis of 1. Damiano,F., Gallerani,R., Liuni,S., Licciulli,F. and Ceci,L.R. (2001) a recombining-repeat-sequence family in the mitochondrial genomes of PLMItRNA, a database for mitochondrial tRNA genes and tRNAs in wheat (Triticum aestivum L.) and rye (Secale cereale L.). Curr. Genet., 23, photosynthetic eukaryotes. Nucleic Acids Res., 29, 167–168. 255–265. 2. Wolff,G., Plante,I., Lang,B.F., Kuck,U. and Burger,G. (1994) Complete 9. Nakazono,M., Tsutsumi,N., Sugiura,M. and Hirai,A. (1995) A small sequence of the mitochondrial DNA of the chlorophyte alga Prototheca repeated sequence contains the transcription initiation sites for both trnfM wickerhamii. Gene content and genome organization. J. Mol. Biol., 237, and rrn26 in rice mitochondria. Plant Mol. Biol., 28, 343–346. 75–86. 10. Kanno,A., Nakazono,M., HiraiA. and Kameya,T. (1997) A chloroplast 3. Turmel,M., Lemieux,C., Burger,G., Lanz,F., Otis,C., Plante,I. and derived trnH gene is expressed in the mitochondrial genome of gramineous Gray,M.W. (1999) The complete mitochondrial DNA sequences of plants. Plant Mol. Biol., 34, 353–356. Nephroselmis olivacea and Pedinomonas minor: two radically different evolutionary patterns within . Plant Cell, 11, 1717–1729.