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The evolutionary conservation of rps3 introns and rps19-rps3-rpl16 gene cluster in Adiantum capillus-veneris mitochondria

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Abstract

Ferns are a large and evolutionarily critical group of vascular land plants for which quite limited mitochondrial gene content and genome organization data are, currently, available. This study reports that the gene for the ribosomal protein S3 (rps3) is preserved and physically clustered to an upstream rps19 and a downstream overlapping rpl16 locus in the mitochondrial DNA of the true fern Adiantum capillus-veneris L. Sequence analysis also revealed that the rps3 gene is interrupted by two cis-splicing group II introns, like the counterpart in lycopod and gymnosperm representatives. A preliminary polymerase chain reaction (PCR) survey confirmed a scattered distribution pattern of both the rps3 introns also in other fern lineages. Northern blot and reverse transcription (RT)–PCR analyses demonstrated that the three ribosomal protein genes are co-transcribed as a polycistronic mRNA and modified by RNA editing. Particularly, the U-to-C type editing amends numerous genomic stop codons in the A. capillus-veneris rps19, rps3 and rpl16 sequences, thus, assuring the synthesis of complete and functional polypeptides. Collectively, the findings from this study further expand our knowledge of the mitochondrial rps3 architecture and evolution, also, bridging the significant molecular data gaps across the so far underrepresented ferns and all land plants.

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Acknowledgments

We thank the Orto Botanico at the Università degli Studi di Napoli and Calabria for kindly made available green leaf tissue from the analyzed plants. We also acknowledge the cooperation with Laszlo Csiba at the Royal Botanic Gardens at Kew (U.K.) for providing some of the DNAs used in this study. Work in the authors’ laboratory was supported by grants from the Università della Calabria and the Italian Ministero dell’Istruzione, Università e Ricerca (M.I.U.R.).

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  1. Dipartimento di Biologia, Ecologia e Scienze della Terra (DiBEST), Università della Calabria, via Ponte P. Bucci, 87036, Arcavacata di Rende, Cosenza, Italy

    Savino Bonavita & Teresa Maria Rosaria Regina

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  1. Savino Bonavita
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  2. Teresa Maria Rosaria Regina
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Correspondence to Teresa Maria Rosaria Regina.

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This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Communicated by M. Kupiec.

This article is dedicated to the memory of Prof. Carla Quagliariello (1949–2012).

Electronic supplementary material

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294_2015_512_MOESM1_ESM.docx

Supplementary material 1 (DOCX 24 kb) Supplemental S1 List of oligonucleotides used as primers for PCR and RT-PCR amplification and sequencing

294_2015_512_MOESM2_ESM.tif

Supplementary material 2 (TIFF 104 kb) Supplemental S2 Nucleotide and derived amino acid sequences of the mitochondrial rps3 gene from A. capillus-veneris. The amino acid sequence is indicated using a single letter abbreviation above the nucleotide sequence. Nucleotides altered by RNA editing, corresponding to C-to-U and U-to-C changes at the RNA level, are indicated in lower-case letters and underlined, whereas the resulting amino acid substitutions (unedited > edited amino acid residues) are given in bold. Vertical arrows indicate the insertion site of the rps3 introns. The position and the orientation of some primers (P1 - P4) used for PCR and RT-PCR amplification and sequencing reactions (see Fig. 1c) are indicated in italic letters and in bold. The A. capillus-veneris nucleotides and amino acids are numbered on the right

294_2015_512_MOESM3_ESM.tif

Supplementary material 3 (TIFF 132 kb) Supplemental S3 RNA secondary structure model of the mitochondrial rps3i1 (a) and rps3i2 (b) introns from A. capillus-veneris. According to Michel et al. (1989), both the two rps3 introns are organized into six well-defined domains (dI–dVI) originating from a central wheel. Exon and intron binding sites (EBS and IBS), the branching point adenosine (marked by an asterisk in domain VI) and the γ-γ′ interactions are indicated. Loops are not drawn to scale and numbers inside the loops indicate their size

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Bonavita, S., Regina, T.M.R. The evolutionary conservation of rps3 introns and rps19-rps3-rpl16 gene cluster in Adiantum capillus-veneris mitochondria. Curr Genet 62, 173–184 (2016). https://doi.org/10.1007/s00294-015-0512-z

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  • DOI: https://doi.org/10.1007/s00294-015-0512-z

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