Skip to main content
Log in

Comparison of mitochondrial and chloroplast genome segments from three onion (Allium cepa L.) cytoplasm types and identification of a trans-splicing intron of cox2

  • Research Article
  • Published:
Current Genetics Aims and scope Submit manuscript

Abstract

To study genetic relatedness of two male sterility-inducing cytotypes, the phylogenetic relationship among three cytotypes of onions (Allium cepa L.) was assessed by analyzing polymorphisms of the mitochondrial DNA organization and chloroplast sequences. The atp6 gene and a small open reading frame, orf22, did not differ between the normal and CMS-T cytotypes, but two SNPs and one 4-bp insertion were identified in CMS-S cytotype. Partial sequences of the chloroplast ycf2 gene were integrated in the upstream sequence of the cob gene via short repeat sequence-mediated recombination. However, this chloroplast DNA-integrated organization was detected only in CMS-S. Interestingly, disruption of a group II intron of cox2 was identified for the first time in this study. Like other trans-splicing group II introns in mitochondrial genomes, fragmentation of the intron occurred in domain IV. Two variants of each exon1 and exon2 flanking sequences were identified. The predominant types of four variants were identical in both the normal and the CMS-T cytotypes. These predominant types existed as sublimons in CMS-S cytotypes. Altogether, no differences were identified between normal and CMS-T, but significant differences in gene organization and nucleotide sequences were identified in CMS-S, suggesting recent origin of CMS-T male-sterility from the normal cytotype.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Abdelnoor RV, Yule R, Elo A, Christensen AC, Meyer-Gauen G, Mackenzie SA (2003) Substoichiometric shifting in the plant mitochondrial genome is influenced by a gene homologous to MutS. Proc Natl Acad Sci 100:5968–5973

    Article  CAS  PubMed  Google Scholar 

  • Abdelnoor RV, Christensen AC, Mohammed S, Munoz-Castillo B, Moriyama H, Mackenzie SA (2006) Mitochondrial genome dynamics in plants and animals: convergent gene fusions of a MutS homologue. J Mol Evol 63:165–173

    Article  CAS  PubMed  Google Scholar 

  • Albert B, Godelle B, Gouyon PH (1998) Evolution of the plant mitochondrial genome: dynamics of duplication and deletion of sequences. J Mol Evol 46:155–158

    Article  CAS  PubMed  Google Scholar 

  • Allen JO, Fauron CM, Mink P, Roark L, Oddiraju S, Lin GN, Meyer L, Sun H, Kim K, Wang C, Du F, Xu D, Gibson M, Cifrese J, Clifton SW, Newton KJ (2007) Comparisons among two fertile and three male-sterile mitochondrial genomes of maize. Genetics 177:1173–1192

    Article  CAS  PubMed  Google Scholar 

  • Arrieta-Montiel M, Lyznik A, Woloszynska M, Janska H, Tohme J, Mackenzie S (2001) Tracing evolutionary and developmental implications of mitochondrial stoichiometric shifting in the common bean. Genetics 158:851–864

    CAS  PubMed  Google Scholar 

  • Backert S, Neilsen BL, Börner T (1997) The mystery of the rings: structure and replication of mitochondrial genomes from higher plants. Trend Plant Sci 2:477–483

    Article  Google Scholar 

  • Bellaoui M, Martin-Canadell A, Pelletier G, Budar F (1998) Low-copy-number molecules are produced by recombination, actively maintained and can be amplified in the mitochondrial genome of Brassicaceae: relationship to reversion of the male sterile phenotype in some cybrids. Mol Gen Genet 257:177–185

    Article  CAS  PubMed  Google Scholar 

  • Berninger E (1965) Contribution à l’étude de la sterilité mâle de l’oignon (Allium cepa L.). Ann Amélior Plant 15:183–199

    Google Scholar 

  • Bonen L (2008) Cis- and trans-splicing of group II introns in plant mitochondria. Mitochondrion 8:26–34

    Article  CAS  PubMed  Google Scholar 

  • Budar F, Touzet P, De Paepe R (2003) The nucleo-mitochondrial conflict in cytoplasmic male sterilities revised. Genetica 117:3–16

    Article  CAS  PubMed  Google Scholar 

  • Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552

    CAS  PubMed  Google Scholar 

  • Engelke T, Terefe D, Tatlioglu T (2003) A PCR-based marker system monitoring CMS-(S), CMS-(T) and (N)-cytoplasm in the onion (Allium cepa L.). Theor Appl Genet 107:162–167

    CAS  PubMed  Google Scholar 

  • Gao LM, Möller M, Zhang XM, Hollingsworth ML, Liu J, Mill RR, Gibby M, Li DZ (2007) High variation and strong phylogeographic pattern among cpDNA haplotypes in Taxus wallichiana (Taxaceae) in China and North Vietnam. Mol Ecol 16:4684–4698

    Article  CAS  PubMed  Google Scholar 

  • Glanz S, Kück U (2009) Trans-splicing of organelle introns—a detour to continuos RNAs. Bioessays 31:921–934

    Article  CAS  PubMed  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Window 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Handa H (2003) The complete nucleotide sequence and RNA editing content of the mitochondrial genome of rapeseed (Brassica napus L.): comparative analysis of the mitochondrial genomes of rapeseed and Arabidopsis thaliana. Nucleic Acids Res 31:5907–5916

    Article  CAS  PubMed  Google Scholar 

  • Hanson MR, Bentolila S (2004) Interactions of mitochondrial and nuclear genes that affect male gametophyte development. Plant Cell 16:S154–S169

    Article  CAS  PubMed  Google Scholar 

  • Havey MJ (1995) Identification of cytoplasms using the polymerase chain reaction to aid in the extraction of maintainer lines from open-pollinated populations of onion. Theor Appl Genet 90:263–268

    Article  CAS  Google Scholar 

  • Havey MJ (2000) Diversity among male-sterility-inducing and male-fertile cytoplasms of onion. Theor Appl Genet 101:778–782

    Article  CAS  Google Scholar 

  • Janska H, Sarria R, Woloszynska M, Arrieta-Montiel M, Mackenzie SA (1998) Stoichiometric shifts in the common bean mitochondrial genome leading to male sterility and spontaneous reversion to fertility. Plant Cell 10:1163–1180

    Article  CAS  PubMed  Google Scholar 

  • Jones HA, Clarke A (1943) Inheritance of male sterility in the onion and the production of hybrid seed. Proc Am Soc Hortic Sci 43:189–194

    Google Scholar 

  • Jones HA, Emsweller SL (1936) A male-sterile onion. Proc Am Soc Hortic Sci 34:582–585

    Google Scholar 

  • Kanazawa A, Tsutsumi N, Hirai A (1994) Reversible changes in the composition of the population of mtDNAs during dedifferentiation and regeneration in tobacco. Genetics 138:865–870

    CAS  PubMed  Google Scholar 

  • Kim S, Lim H, Park S, Cho K, Sung S, Oh D, Kim K (2007) Identification of a novel mitochondrial genome type and development of molecular makers for cytoplasm classification in radish (Raphanus sativus L.). Theor Appl Genet 115:1137–1145

    Article  CAS  PubMed  Google Scholar 

  • Kim S, Lee E, Cho DY, Han T, Bang H, Patil BS, Ahn YK, Yoon M (2009a) Identification of a novel chimeric gene, orf725. and its use in development of a molecular marker for distinguishing among three cytoplasm types in onion (Allium cepa L.). Theor Appl Genet 118:433–441

    Article  CAS  PubMed  Google Scholar 

  • Kim S, Lee Y, Lim H, Ahn Y, Sung S (2009b) Identification of highly variable chloroplast sequences and development of cpDNA-based molecular markers that distinguish four cytoplasm types in radish (Raphanus sativus L.). Theor Appl Genet 119:189–198

    Article  CAS  PubMed  Google Scholar 

  • Kmiec B, Woloszynska M, Janska H (2006) Heteroplasmy as a common state of mitochondrial genetic information in plants and animals. Curr Genet 50:149–159

    Article  CAS  PubMed  Google Scholar 

  • Knoop V (2004) The mitochondrial DNA of land plants: peculiarities in phylogenetic perspective. Curr Genet 46:123–139

    Article  CAS  PubMed  Google Scholar 

  • Kubo T, Newton KJ (2008) Angiosperm mitochondrial genomes and mutations. Mitochondrion 8:5–14

    Article  CAS  PubMed  Google Scholar 

  • Kubo T, Nishizawa S, Sugawara A, Itchoda N, Estiati A, Mikami T (2000) The complete nucleotide sequence of the mitochondrial genome of sugar beet (Beta vulgaris L.) reveals a novel gene for tRNAcys(GCA). Nucleic Acids Res 28:2571–2576

    Article  CAS  PubMed  Google Scholar 

  • Kudla J, Albertazzi FJ, Blazevic D, Hermann M, Bock R (2002) Loss of the mitochondrial cox2 intron 1 in a family of monocotyledonous plants and utilization of mitochondrial intron sequences for the construction of a nuclear intron. Mol Genet Genomics 267:223–230

    Article  CAS  PubMed  Google Scholar 

  • Lee Y, Park S, Lim C, Kim H, Lim H, Ahn Y, Sung S, Yoon M, Kim S (2008) Discovery of a novel cytoplasmic male-sterility and its restorer lines in radish (Raphanus sativus L.). Theor Appl Genet 117:905–913

    Article  PubMed  Google Scholar 

  • Mackenzie SA, Chase CD (1990) Fertility restoration is associated with loss of a portion of the mitochondrial genome in cytoplasmic male-sterile common bean. Plant Cell 2:905–912

    Article  CAS  PubMed  Google Scholar 

  • Meng L, Yang R, Abbott RJ, Miehe G, Hu T, Liu J (2007) Mitochondrial and chloroplast phylogeography of Picea crassifolia Kom. (Pinaceae) in the Qinghai-Tibetan plateau and adjacent highlands. Mol Ecol 16:4128–4137

    Article  CAS  PubMed  Google Scholar 

  • Notsu Y, Masood S, Nishikawa T, Kubo N, Akiduki G, Nakazono M, Kirai A, Kadowaki K (2002) The complete sequence of the rice (Oryza sativa L.) mitochondrial genome: frequent DNA sequence acquisition and loss during the evolution of flowering plants. Mol Genet Genomics 268:434–445

    Article  CAS  PubMed  Google Scholar 

  • Ohsako T, Wang G, Miyashita NT (1996) Polymerase chain reaction-single strand conformational polymorphism analysis of intra- and interspecific variations in organellar DNA regions of Aegilops mutica and related species. Genes Genet Syst 71:281–292

    Article  CAS  PubMed  Google Scholar 

  • Oldenburg DJ, Bendich AJ (2001) Mitochondrial DNA from the Liverwort Marchantia polymorpha: circularly permuted linear molecules, head-to-tail concatemers, and a 5′ protein. J Mol Biol 310:549–562

    Article  CAS  PubMed  Google Scholar 

  • Palmer JD (1988) Intraspecific variation and multicircularity in Brassica mitochondrial DNAs. Genetics 118:341–351

    CAS  PubMed  Google Scholar 

  • Palmer JD, Herbon LA (1987) Unicircular structure of the Brassica hirta mitochondrial genome. Curr Genet 11:565–570

    Article  CAS  PubMed  Google Scholar 

  • Pyle AM, Fedorova O, Waldsich C (2007) Folding of group II introns: a model system for large, multidomain RNAs? Trend Biochem Sci 32:138–145

    Article  CAS  PubMed  Google Scholar 

  • Qiu Y, Palmer JD (2004) Many independent origins of trans splicing of a plant mitochondrial group II intron. J Mol Evol 59:80–89

    CAS  PubMed  Google Scholar 

  • Reboud X, Zeyl C (1993) Organelle inheritance in plants. Heredity 72:132–140

    Article  Google Scholar 

  • Sakai T, Imamura J (1993) Evidence for a mitochondrial sub-genome containing radish Atp1 in a Brassica napus cybrid. Plant Sci 90:95–103

    Article  CAS  Google Scholar 

  • Sandhu AS, Abdelnoor RV, Mackenzie SA (2007) Transgenic induction of mitochondrial rearrangements for cytoplasmic male sterility in crop plants. Proc Natl Acad Sci 104:1766–1770

    Article  CAS  PubMed  Google Scholar 

  • Sato Y (1998) PCR amplification of CMS-specific mitochondrial nucleotide sequences to identify cytoplasmic genotypes of onion (Allium cepa L.). Theor Appl Genet 96:367–370

    Article  CAS  Google Scholar 

  • Satoh M, Kubo T, Nishizawa S, Estiati A, Itchoda N, Mikami T (2004) The cytoplasmic male-sterile type and normal type mitochondrial genomes of sugarbeet share the same complement of genes of known function but differ in the content of expressed ORFs. Mol Gen Genomics 272:247–256

    Article  CAS  Google Scholar 

  • Schweisguth B (1973) Étude d’un nouveau type de stérilité male chez l’oignon, Allium cepa L. Ann Amélior Plant 23:221–233

    Google Scholar 

  • Shedge V, Arrieta-Montiel M, Christensen AC, Mackenzie SA (2007) Plant mitochondrial recombination surveillance requires unusual RecA and MutS homologs. Plant Cell 19:1251–1264

    Article  CAS  PubMed  Google Scholar 

  • Small I, Suffolk R, Leaver CJ (1989) Evolution of plant mitochondrial genomes via substoichiometric intermediates. Cell 58:69–76

    Article  CAS  PubMed  Google Scholar 

  • Sugiyama Y, Watase Y, Nagase M, Makita N, Yagura S, Hirai A, Sugiura M (2005) The complete nucleotide sequence and multipartite organization of the tobacco mitochondrial genome: comparative analysis of mitochondrial genomes in higher plants. Mol Gen Genomics 272:603–615

    Article  CAS  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  CAS  PubMed  Google Scholar 

  • Toor N, Keating KS, Taylor SD, Pyle AM (2008) Crystal structure of a self-spliced group II intron. Science 320:77–82

    Article  CAS  PubMed  Google Scholar 

  • Unseld M, Marienfeld JR, Brandt P, Brennicke A (1997) The mitochondrial genome of Arabidopsis thaliana contains 57 genes in 366, 924 nucleotides. Nature genet 15:57–61

    Article  CAS  PubMed  Google Scholar 

  • Ward BL, Anderson RS, Bendich AJ (1981) The mitochondrial genome is large and variable in a family of plants (Cucurbitaceae). Cell 25:793–803

    Article  CAS  PubMed  Google Scholar 

  • Woloszynska M, Trojanowski D (2009) Counting mtDNA molecules in Phaseolus vulgaaris: sublimons are constantly produced by recombination via short repeats and undergo rigorous selection during substoichiometric shifting. Plant Mol Biol 70:511–521

    Article  CAS  PubMed  Google Scholar 

  • Zaegel V, Guermann B, Le Ret M, Andrés C, Meyer D, Erhardt M, Canaday J, Gualberto JM, Imbault P (2006) The plant-specific ssDNA binding protein OSB1 is involved in the stoichiometric transmission of mitochondrial DNA in Arabidopsis. Plant Cell 18:3548–3563

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This study was supported by the Specific Joint Agricultural Research-Promoting Projects (Project No. 200803A01081219), RDA, Republic of Korea, and by the Biotechnology Research Institute, Chonnam National University, Republic of Korea. We thank Seon Chong and Mi-Young Kim for their dedicated technical assistance.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sunggil Kim.

Additional information

Communicated by R. Bock.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kim, S., Yoon, MK. Comparison of mitochondrial and chloroplast genome segments from three onion (Allium cepa L.) cytoplasm types and identification of a trans-splicing intron of cox2 . Curr Genet 56, 177–188 (2010). https://doi.org/10.1007/s00294-010-0290-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00294-010-0290-6

Keywords

Navigation